Combination of Ultrasonographic and Thermographic Assessments for Predicting Partial-thickness Pressure Ulcer Healing

Index: WOUNDS 2011;23(9):285–292

  Abstract: The ability to predict the prognosis of a pressure ulcer is re¬quired to establish appropriate management in the early phase. The present study reports the usefulness of a combined assessment tech¬nique using ultrasonography and thermography for predicting delayed wound healing. Methods. This retrospective cohort study included 37 patients with Stage I or II pressure ulcers. The patients were followed up for at least 3 weeks. The ultrasonographic and thermographic as¬sessments were conducted at the initial multidisciplinary team round. The presence of four ultrasonographic features (unclear layered struc¬ture, hypoechoic lesion, discontinuous fascia, and heterogeneous hy¬poechoic area) and one thermographic feature (increased temperature) were determined from within the wound bed. Wound healing was re¬assessed after 2 weeks and the rate of area reduction was calculated to determine whether the pressure ulcer was healing properly. A mul¬tivariate logistic analysis was used to assess the predictive values of the possible assessment features. Results. A comprehensive review of the ultrasonographic and thermographic assessments of the pressure ulcers found that the combination of unclear layered structure and increased temperature was beneficial for predicting wound healing. When a pressure ulcer presented with an unclear layered structure and increased temperature in the wound bed, the risk of delayed wound healing or wound deterioration was 6.85 times higher compared with a pressure ulcer that did not have these manifestations. Conclusion. The combination of ultrasonographic and thermographic assessments facilitates precise prediction of pressure ulcer outcomes.   Pressure ulcers commonly occur not only in older people and individuals with spinal cord injuries, but also in patients hospitalized in acute care settings.^1–6 Since the pathophysiology of pressure ulcers that acutely occur in these settings changes dramatically during the wound healing course, it is difficult to precisely assess wound status in the early phase. Establishing an appropriate care strategy is required based on wound assessment in situations where many patients with pressure ulcers are discharged with unhealed wounds because of shortened lengths of hospitalization.⁷ Indeed, it was reported that 22% of patients were discharged with unhealed pressure ulcers, which hinders the acceptance of patients in community care settings.⁸ There are several wound assessment tools for evaluating the severity of pressure ulcers from multi-dimensional aspects. It has been reported that these assessment scales can be used to predict pressure ulcer healing.   However, some of these assessment tools are based on visual and subjective assessments, and it is therefore difficult to evaluate the subcutaneous status, which provides clues for assessing deep tissue damage or subtle inflammation—an important sign of delayed wound healing.⁹   The authors have previously reported several methods, including ultrasonographic assessment and thermographic assessment.^10–12 Ultrasonographic assessment is useful for evaluating deep tissue damage or inflammatory edema underneath the skin.^10–12 The authors identified unique ultrasonographic signs for the superficial and deep tissues including unclear layered structure (ULS), hypoechoic lesion (HL), discontinuous fascia (DF), and heterogeneous hypoechoic area (HHA).¹² The authors were able to predict the future progression of pressure ulcers by using these signs. Meanwhile, thermographic assessment can be used to evaluate the inflammatory status of the wound bed because the device can visually display temperature distribution.¹³ It was assumed that the temperature in the wound bed would increase when subtle inflammation occurred, even though the wound did not show any visually detectable inflammatory signs, and found that wounds with higher temperatures within the wound bed compared to surrounding tissue have a 2.23-fold higher risk for delayed wound healing compared with wounds with lower temperatures within the wound bed.¹³   Based on these observations, the authors were able to predict the progression to full-thickness pressure ulcers or delayed wound healing by evaluating subtle inflammation or deep tissue injury using these devices. However, these assessment techniques sometimes fail to predict pressure ulcer prognosis, and studies using these assessment techniques to assess Stage I pressure ulcers have not been undertaken until this point. Since the authors routinely assess pressure ulcers using these devices, it was hypothesized that the combination of ultrasonographic and thermographic assessments would be more useful for predicting the prognosis of pressure ulcers at the time of initial assessment. The present study explores the optimal combination of ultrasonographic and thermographic assessments and investigates its effectiveness in acute care settings.   

Methods

  Study design. This retrospective cohort study was conducted at The University of Tokyo Hospital with approval from the local Institutional Review Board. Patients with Stage I or II pressure ulcers (partial-thickness pressure ulcers) on their trunk were included if they were treated by the multidisciplinary pressure ulcer team for at least 3 weeks or until the pressure ulcer healed, and received both ultrasonographic and thermographic assessments at initial presentation. Patients with severe medical conditions were excluded, including terminal conditions or circulatory shock, and/or had pressure ulcers located on the extremities.   A total of 37 patients were recruited during the study period from April 2007 to July 2011 (Table 1). Ten patients had Stage I pressure ulcers and 27 had Stage II pressure ulcers, graded according to the National Pressure Ulcer Advisory Panel guidelines.¹⁴ Nineteen patients had pressure ulcers on the sacral region.   Wound assessment. Pressure ulcer severity was evaluated by DESIGN-R, which is a 7-item monitoring system that evaluates pressure ulcer status: Depth, Exudate, Size, Inflammation/infection, Granulation tissue, and Necrotic tissue.¹⁵ The scores ranged from 0 to 66, and higher DESIGN-R scores indicated more severe wound statuses. The validity and reliability of this tool have been confirmed.¹⁶   The multidisciplinary team recorded wound areas by taking digital photographs at the initial presentation and 2 weeks afterward. The wound reduction rate (%) was calculated as follows: Wound reduction rate (%) = (baseline area – area at week 2) / baseline area × 100. Pressure ulcers with a wound area reduction of 20% or greater compared with baseline after 2 weeks were considered to be healing normally, while pressure ulcers with no changes or an increase in wound area or progression to more severe stages despite optimal treatment were considered to have delayed healing. This percentage was based on guidance in a previous study, which reported that patients who fail to show at least a 40% reduction in ulcer size after 4 weeks of therapy should be re-evaluated and considered for other treatments.¹⁷   Ultrasonographic assessment. A portable ultrasound system with a 10-MHz probe (LOGIQ Book XP; GE Healthcare, Chalfont St. Giles, UK) was used. The transducer was attached just above the wound site in a horizontal and vertical manner. Four ultrasonographic features were evaluated: ULS, HL, DF, and HHA.¹² ULS is a subcutaneous condition that does not show a clear layered structure, such as a subcutaneous fatty layer, superficial fascia, deep fascia, muscular layer, bursa, and bone (periosteum). A ULS usually has a foggy-appearing area with low contrast and rough resolution. An HL is a small lesion with a relatively clear margin that has little or no echoic signal and may correspond to a nonvascularized area such as a hematoma, seroma, or necrotic tissue. A DF is an interrupted high-signal line corresponding to the superficial or deep fascia that probably reflects a damaged, disrupted, or ruptured fascia. An HHA is a round or oval area with a heterogeneous internal echo that disrupts the normally layered structure. An HHA sometimes has a diffuse border. All images were evaluated if several ultrasonographic images were captured at the initial multidisciplinary team assessment.   Thermographic assessment. To assess the wound bed temperatures, thermographic images of the wound bed and periwound skin were captured using an infrared thermograph (Thermotracer TH5108ME, NEC Avio Infrared Technology Co. Ltd, Tokyo, Japan). Its measurable range was 0–70˚C, with an error range of ± 0.7˚C and an accuracy of 0.1˚C. This device has been used in previous clinical studies.¹⁸ Unlike a previous study that assessed the usefulness of thermographic assessment for predicting delayed wound healing in Stage II to IV pressure ulcers,¹³ the present study also included Stage I pressure ulcers, which made it necessary to reestablish the assessment features. In Stage II pressure ulcers, the wound bed is generally exposed to air and thus the temperature of the wound bed is decreased compared with the intact skin surrounding the wound, which may be caused by evaporation of the exudate. Therefore, the authors defined that the same temperature in the wound bed compared with the surrounding skin indicated a temperature increase in the wound bed. Conversely, in Stage I ulcers, the temperature distribution is quite different from Stage II or more severe wounds. Stage I pressure ulcers exist within the epidermis and thus do not produce exudate, leading to no remarkable difference in temperature between the wound site and surrounding skin. In the case of inflammation, the temperature of the wound site is increased. In summary, an increased or equal temperature in the wound bed in Stage II pressure ulcers and an increased temperature in the wound site in Stage I pressure ulcers were indicative features of inflammation and was designated as “increased temperature.”   

Statistical Analysis

  The proportions of patients with positive or negative results for ultrasonographic and thermographic assessments with the healing outcomes were compared using the chi-square test or Fisher’s exact probability test. Based on these results, the optimal combination of ultrasonographic and thermographic features was determined. The risk of the new assessment indicator for delayed wound healing was calculated using a multivariate logistic regression analysis with adjustment for covariates that could affect the wound healing. To assess the predictive usefulness of a high temperature, the sensitivity, specificity, positive predictive value, and negative predictive value were calculated. All statistical analyses were performed using Statistical Analysis System Version 9.1 (SAS Institute Inc, Cary, NC).   

Results

  Among the 37 patients, 13 pressure ulcers healed completely, 11 were in the process of healing, and 13 showed delayed healing or deterioration. At the initial ultrasonographic assessment, 31 pressure ulcers were positive for ULS, 10 for HL, 14 for DF, and one for HHA. Only ULS had the potential to predict the pressure ulcer prognosis (P = 0.072, Table 2). Alternatively, 19 pressure ulcers were judged to have increased temperature by the thermographic assessment, and these pressure ulcers tended to be in the delayed healing or deteriorated categories (P = 0.109, Table 3). Based on these results, ULS and increased temperature were combined for predicting wound prognoses. Four combinations of positive or negative ULS and increased or no increased temperature were set and tabulated with the wound prognosis (Table 4). The results showed that negative ULS and/or no increased temperature were related to the healing or healed pressure ulcers. The combination of positive ULS and increased temperature was defined as a new assessment indicator for pressure ulcer prognosis with the assumption that positive ULS and increased temperature indicated inflammation. The pressure ulcers that were positive for the new assessment indicator showed a significantly higher proportion in the delayed healing or deteriorated pressure ulcers (P = 0.036, Table 5). After adjusting for age, initial wound area, and initial total DESIGN-R score, which could affect healing, the new assessment indicator was significantly associated with delayed healing or deteriorated pressure ulcers (adjusted odds ratio: 6.85, 95% confidence interval: 1.11–42.13, P = 0.038, Table 6). The sensitivity was 0.69, the specificity was 0.71, the positive predictive value was 0.56, and the negative predictive value was 0.81.   

Case Reports

  Case 1: Deteriorated pressure ulcer with positive ULS and increased temperature.   A 54-year-old woman had a Stage II pressure ulcer at the coccyx area. The pressure ulcer was already present at the time of admission to hospital. She had multiple sclerosis, glaucoma, and type 2 diabetes mellitus. The initial pressure ulcer area was 1.42 cm² with a total DESIGN-R score of 7. Ultrasonographic assessment showed positive ULS, negative HL, negative DF, and negative HHA (Figure 1). Thermographic assessment showed marked increase in temperature within the wound bed. The pressure ulcer had deteriorated to Stage III after 2 weeks of follow up.   Case 2: Healed pressure ulcer with negative ULS and no increased temperature.   An 85-year-old woman presented with a Stage II pressure ulcer at the right greater trochanter and was also suffering from dehydration and hypothermia. A viscoelastic mattress was used to manage interface pressure. The initial pressure ulcer area was 1.14 cm² with a total DESIGN-R score of 7. Ultrasonographic assessment showed negative ULS, negative HL, negative DF, and negative HHA (Figure 2). Thermographic assessment showed no increase in temperature within the wound bed. The pressure ulcer healed within 1 week.   

Discussion

  This study has proposed a novel assessment indicator for delayed pressure ulcer healing by combining thermographic and ultrasonographic assessments. The combination of positive ULS and increased temperature in the wound bed is a promising indicator, and can easily be assessed in the clinical setting using common devices. Based on these methods, a more precise assessment can be carried out at the early phase of the pressure ulcer course, which would enable the determination of an appropriate treatment strategy. Generally, ultrasonographic assessment requires mastery to understand the ultrasonographic images. However, ULS can be relatively easy to detect within the superficial layer, as shown in Case 1, compared with the other three ultrasonographic features.   ULS indicates edema, water restoration, or destruction of the superficial structure, which can also be presented during the normal wound healing process. Many pathological processes influence ultrasonographic features, and it is sometimes difficult to detect the cause of the manifestation. In combination with a thermographic assessment, inflammatory edema can be detected using the new assessment indicators of increased temperature and positive ULS. Combining ultrasonographic and thermographic assessments can provide pathological understanding and reduces the risk of misunderstanding of the ultrasonographic findings, but thermographic assessment also requires careful consideration. As previously reported, thermography should generally be carried out in a temperature-conditioned room to minimize any environmental effects.¹³ The authors previously established a thermographic assessment method for pressure ulcer assessment involving relative comparisons between the wound bed and the surrounding skin, which diminishes the environmental effects on the temperature. In the present study, a relative increase in the wound bed temperature was regarded as an inflammatory sign. Although the thermographic assessment provides useful indications for the detection of subtle inflammation, a temperature change alone may not only reflect inflammation. With that in mind, the combination of ultrasonographic and thermographic assessments provides greater understanding of the pathophysiology.   Nishide et al¹⁹ reported that the indicators for inflammation of the callus included increased temperature and subcutaneous edema. The present retrospective cohort study also revealed that the combination of increased temperature and ULS as an edematous ultrasonographic feature was a good indicator of inflammation resulting in delayed wound healing. As shown in the case reports, the initial wound areas and initial DESIGN-R scores did not differ, but the ultrasonographic and thermographic assessments revealed clear differences. The gross assessments are basically based on visual assessments, which have the risk of underscoring subtle inflammatory responses or underlying changes within the deep tissue. The technology-based assessment strategies provide additional information to the visual assessments, resulting in a better predictive capacity for wound healing.   Previously, the authors reported the usefulness of technology-based assessments, including ultrasonography and thermography.^12,13 The assessment focus of the present study was fundamentally based on these previous reports. The targets of the present study were Stage I and II pressure ulcers associated with superficial skin damage, which makes it difficult to compare the predictive capacity directly with previous reports, which included full-thickness pressure ulcers.^12,13 However, this new combined assessment indicator provides more precise prognostic values, especially for the negative predictive value.   The clinical implications of this study are that if a clinician observes a clear, superficial layer structure and/or no increase in the temperature of the wound bed, the probability of a delay in wound healing or deterioration of the pressure ulcer is about 20%, and thus the clinician does not need to change the pressure ulcer management course. If the layer structure becomes unclear and the wound bed temperature is increased, it is wise to change the management course in order to reduce inflammation.   

Conclusion

  This study included a smaller number of patients with deep tissue injuries, and thus, the predictive capacity of the combined assessment indicator for these patients was not investigated. Owing to the limited follow-up duration and the differences in the wound healing phases among individuals, these technology-based assessments represent different pathophysiologies. Based on these limitations, it is noteworthy that these assessment technologies could predict the pressure ulcers that would heal or not heal after 2 weeks.   Future studies should investigate biological assessment indicators since the cause of inflammation detected by the ultrasonographic and thermographic assessments cannot be determined at the present time. Combination with a biological assessment that is able to differentiate between inflammation caused by an external force or infection will serve as a comprehensive pressure ulcer assessment tool.   

References

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