Background: Ultrasonography may have potential as an effective diagnostic tool for deep tissue injury (DTI) in tissues overlying bony prominences that are vulnerable when under sustained loading in sitting. Methods: Three cases of DTI in the fat and muscle layers overlying the ischial tuberosity of the pelvis in 3 persons with spinal cord injury (SCI) with different medical histories and abnormal tissue signs are described. Conclusion: There is a need for prospective studies using a reliable standardized ultrasonography protocol to diagnose DTI and to follow its natural history to determine its association with the development of pressure injuries.
International clinical practice guidelines on the prevention and treatment of pressure injuries (PI) include suspected deep tissue injury (DTI) in the PI classification system.1 The clinical sign of DTI refers to skin changes on visual inspection (a purple or maroon localized area of discolored intact skin or blood-filled blister) and/or by palpation that are considered to indicate damage to the underlying soft tissues due to pressure. Guidelines do not require medical imaging to confirm this tissue damage nor do they recommend imaging for early detection. DTI may evolve into an open wound or may resolve without tissue loss.2,3 DTI and PI are serious and common complications in neurological conditions such as spinal cord injury (SCI). This patient group has a pressure injury incidence ranging from 23% to 33% per year with a lifetime risk of 85%4,5 and a DTI prevalence ranging from 7% to 85%.6–8
Ultrasound is portable, available, and safe, and it can be used to detect DTI in real time.2,3,6–9 This modality has been used to detect DTI prior to any observable changes in skin tissues.2 Accordingly, ultrasound may enable earlier and cost-effective detection of preclinical injury, prompt early intervention, and potentially prevent progression to an open wound.10 The most critical early intervention is offloading the area immediately.11–13 Once offloaded, root cause analysis of the PI can be planned and additional early intervention can be provided.13 For sitting-acquired PIs, this includes individualized postural and assistive technology assessment with provision of optimal sitting support surfaces such as a wheelchair cushion.12,14
Ultrasound has been used to image normal tissue layers overlying the ischial tuberosity (IT) of the buttocks (Figure 1a) and identify abnormal signs in the soft tissue layers of the buttocks in persons with SCI; however, no details of the ultrasound protocol or patients' medical history have been provided in this literature.2,6–8,15,16 To date, 4 DTI findings on ultrasound have been described as distinct types of abnormal tissue: an unclear layered structure, a hypoechoic lesion, a discontinuous superficial or deep fascia, and a heterogeneous hypoechoic area.2 A hypoechoic lesion in SCI is believed to be diagnostic of a DTI.6 Following the natural history of DTI provides additional information on which temporal patterns can be identified as reliable predictors of progression to an open wound. The aims of this article are to describe the utility of ultrasound in 3 cases of DTI in persons with SCI, specifically the abnormal signs, the location in the soft tissue layers, and the importance of medical histories in the imaging diagnosis. The CARE guidelines were followed for this report,17 the study was approved by the Institutional Review Board, and informed consent was obtained.
(a) Ultrasound image of an able-bodied participant sitting upright on a cut-out seat with soft tissues of the buttocks unloaded, using 3–12 MHz linear probe demonstrates the layers overlying the lowest point of the IT (arrow), conjoint tendon of the long head of the biceps femoris and the semitendinosus muscles (T), gluteus maximus muscle (G), and subcutaneous fat (F) layer with skin at top. Corresponding schematic image of these same layers is on the right. (b) Case 1: peak interface pressures ≥200 mm Hg under both ischial tuberosities (ITs) in loaded sitting on a custom planar foam wheelchair cushion measured 6 months prior to the abnormal soft tissue changes. (c) 6–15 MHz linear probe image obtained in side lying with knees flexed to 100° depicts the abnormal fluid collection (thick hypoechoic pseudo capsule with possible calcification) in the fat layer (F). Gluteus muscle (G) layer is intact. (d) In transverse view, 6–15 MHz color Doppler ultrasound of the fat layer shows red and blue signals that indicate increased vascularity peripherally and a hypovascular pattern centrally within the abnormal tissue.
(a) Ultrasound image of an able-bodied participant sitting upright on a cut-out seat with soft tissues of the buttocks unloaded, using 3–12 MHz linear probe demonstrates the layers overlying the lowest point of the IT (arrow), conjoint tendon of the long head of the biceps femoris and the semitendinosus muscles (T), gluteus maximus muscle (G), and subcutaneous fat (F) layer with skin at top. Corresponding schematic image of these same layers is on the right. (b) Case 1: peak interface pressures ≥200 mm Hg under both ischial tuberosities (ITs) in loaded sitting on a custom planar foam wheelchair cushion measured 6 months prior to the abnormal soft tissue changes. (c) 6–15 MHz linear probe image obtained in side lying with knees flexed to 100° depicts the abnormal fluid collection (thick hypoechoic pseudo capsule with possible calcification) in the fat layer (F). Gluteus muscle (G) layer is intact. (d) In transverse view, 6–15 MHz color Doppler ultrasound of the fat layer shows red and blue signals that indicate increased vascularity peripherally and a hypovascular pattern centrally within the abnormal tissue.
Case 1: Ultrasound As a Behavior Change Technique to Enhance Self-management
A 38-year-old male had a T12 SCI, American Spinal Injury Association Impairment Scale (AIS A) incurred 11 years previously following a motor vehicle accident. He was preparing for a hand-cycling marathon using a hand cycle without a cushion and reported a palpable swollen area and nonblanchable redness overlying his left ischial IT. He was admitted to a spinal cord rehabilitation unit for bed rest to offload the ITs. There were no signs of infection, and the lesion was aspirated on 3 occasions with a total of 59 mL of straw-colored fluid withdrawn from the lesion. After the third aspiration, a portable ultrasound examination (LOGIQ, General Electric Healthcare, Little Chalfont, UK) using a 6–15 MHz linear probe with MSK General preset revealed an area of 45 × 33 × 18 mm with a thick hypoechoic pseudo capsule and possible calcification or ossification in the fat layer (Figure 1c). Vascularity assessment using color Doppler flow imaging was used to complement the final diagnosis16 as the fat layer showed increased vascularity peripherally and a hypovascular pattern centrally within the abnormal tissue (Figure 1d).
Interface pressure mapping (X3, Xsensor Technology Corp., Calgary, Canada) was performed on the patient's own wheelchair cushion in his manual wheelchair 6 months prior to the ultrasound assessment as part of a research study (Figure 1b). Of a total of 1,200 interface pressure mapping (IPM) frames recorded, 200 were deleted due to movement artifacts and the remaining 1,000 frames were averaged. Results revealed high mean peak interface pressures (≥200 mm Hg) under both ITs with mean total seat contact area of 1109 cm2 of a maximum 1296 cm2 (85.6% of the 36 × 36 cm wheelchair cushion) and high pressure gradients surrounding the peak pressures corresponding to his ITs.
His wheelchair seating was reviewed and a new planar foam cushion was provided. He was discharged after 4 weeks in hospital when he privately purchased an air-cell wheelchair cushion for his hand cycle based on the ultrasound and IPM results. He added palpation of these bony areas to his regular skin checks, particularly after episodes of cycling. The natural history of this DTI resulted in no open wound. This case describes the strategy of providing information to the patient about their abnormal ultrasound in combination with their IPM as a behavior change technique for promoting more effective self-management.
Case 2: Ultrasound Used to Regularly Monitor DTI Status
A 52-year-old female had a T12/L1 injury, AIS B, 37 years previously, following a motor vehicle accident. Over the 4 days prior to admission, she developed symptoms consistent with infection: fever and rigors, abnormal sensations in her legs, swelling and rash over her left thigh and buttock, and inguinal lymphadenopathy. She reported pins and needles, cramp-like sensations, and shocks down both legs. She was admitted to hospital with a diagnosis of cellulitis overlying a mass on her left buttock. On ultrasound (HDI 5000, Phillips Electronics North America Corporation, Andover, MA) using a 2–5 MHz curvilinear probe with abdominal-general preset, there was a generalized heterogeneous echo texture, with hyperechogenicity within the more superficial fat consistent with edema or inflammatory change. A subsequent CT scan confirmed a poorly defined area of inflammatory change in the subcutaneous fat medial to the hamstring tendons and gluteus maximus in the left buttock overlying the IT with a region (72 × 60 × 68 mm) demonstrating increased attenuation (Figure 2a). The transverse CT image depicts this subcutaneous fat DTI on both the left and right and dystrophic calcifications in the subcutaneous fat layer that are nonspecific, but one cause is fat necrosis. She was treated with bed rest and intravenous antibiotics. She returned to sitting, although no wheelchair or seating assessment was performed as they were not ordered by the attending physician; however, she did have repeated ultrasound imaging of the DTI to measure change. She was hospitalized for 3 months. At the time of discharge, the ultrasound imaging (2–5 MHz curvilinear probe using abdominal-general preset) revealed unresolved features. There was a complex cystic collection in the subcutaneous fat layer, with areas of anechoic (fluid) and solid/soft tissue echotexture from the left IT to the intact skin (3.7 × 43 × 4.4 mm) (Figure 2c) and a loaded sitting ultrasound image showed the DTI extends the full length of the left IT (Figure 2d). Case 2 highlights the application of ultrasound to monitor changes in a DTI over time.
(a) Case 2: CT scan in sagittal plane demonstrating increased attenuation in subcutaneous (fat) medial to the hamstring tendons and gluteus maximus in the left buttock (arrow) overlying the ischial tuberosity (IT) (72 × 60 × 68 mm). (b) Transverse CT depicts this subcutaneous fat deep tissue injury (DTI) on the left and right (arrows) and dystrophic calcification in the subcutaneous fat layer, which is nonspecific, but one cause is fat necrosis (arrowhead). (c) Upon discharge, patient sitting upright on a cut-out cushion with soft tissues unloaded. Ultrasound image (2–5 MHz curvilinear probe using abdominal-general preset) demonstrates a complex cystic collection in the fat layer with areas of anechoic (fluid) and solid/soft tissue echotexture from the IT to the intact skin (3.7 × 43 × 4.4 mm) (arrow) overlying the left IT (arrowhead) in the long axis. (d) Patient now sitting upright on water cushion with the soft tissues loaded. Ultrasound image using same probe and settings confirms the subcutaneous (fat) DTI overlies the IT along its length (arrowhead).
(a) Case 2: CT scan in sagittal plane demonstrating increased attenuation in subcutaneous (fat) medial to the hamstring tendons and gluteus maximus in the left buttock (arrow) overlying the ischial tuberosity (IT) (72 × 60 × 68 mm). (b) Transverse CT depicts this subcutaneous fat deep tissue injury (DTI) on the left and right (arrows) and dystrophic calcification in the subcutaneous fat layer, which is nonspecific, but one cause is fat necrosis (arrowhead). (c) Upon discharge, patient sitting upright on a cut-out cushion with soft tissues unloaded. Ultrasound image (2–5 MHz curvilinear probe using abdominal-general preset) demonstrates a complex cystic collection in the fat layer with areas of anechoic (fluid) and solid/soft tissue echotexture from the IT to the intact skin (3.7 × 43 × 4.4 mm) (arrow) overlying the left IT (arrowhead) in the long axis. (d) Patient now sitting upright on water cushion with the soft tissues loaded. Ultrasound image using same probe and settings confirms the subcutaneous (fat) DTI overlies the IT along its length (arrowhead).
Case 3: Ultrasound Used to Confirm Imaging Diagnosis and Monitor DTI
A 62-year-old male had a L1 lesion, AIS A, due to an anterior spinal artery infarct sustained 6 months previously. He was admitted to hospital with a large pulmonary embolus and had an emergency embolectomy. This was complicated by cardiac arrest and development of atrial fibrillation for which he was anticoagulated with warfarin. Three weeks after transfer to the rehabilitation unit, he had a CT scan of the abdomen and pelvis to investigate anemia (Figure 3a). This identified a large mass in his left gluteus medius muscle that was relatively dense and extended into the gluteus maximus compartment lower down. Given the patient's medical history, the imaging diagnosis was identified as a recent hematoma (170 × 71 mm). In the same CT, a subcutaneous (fat) DTI was noted on the right (Figure 3a). On repeat CT, the medical notes reported there was a size reduction of the left hematoma (Figure 3b); however, measurement was difficult given the similarities in density of the hematoma and adjacent gluteus muscle. Ultrasound was able to more accurately assess the size of the hematoma, which was estimated to be 41 × 20 mm (not shown), using a 4–7 MHz linear probe (HDI5000, Phillips Electronics North America Corporation, Andover, MA). The repeat CT scan also reported the right fat DTI was still present. An ultrasound confirmed a hypoechoic area was consistent with a hematoma overlying the right IT in the fat layer estimated to be 8 × 15 × 18 mm (Figure 3c). He was treated with bed rest to offload and had repeated ultrasounds to monitor the hematoma. At this time, he was also pressure mapped (FSA, Vista Medical, Winnipeg, Canada) as part of a research study. The peak interface pressure under the right IT was ≥200 mm Hg and his left was 161 mm Hg (Figure 3d). Pressure gradients were high surrounding both ITs, with the right greater than the left. He was discharged after 3 months with intact skin and sitting in his original wheelchair seating system.
(a) Case 3: CT scan on admission demonstrates a large (170 × 71 mm) recent hematoma in the gluteus medius of the left buttocks (arrowhead). On the right, there is a subcutaneous (fat) deep tissue injury (DTI; box). The arrow is positioned at the most medial extent of the gluteus maximus muscle; everything medial to it is the fat DTI. (b) The CT scan 1 month later is captured at a higher level than the original scan (a); however, medical notes indicate a decrease in the size of the left hematoma in the gluteus medius (arrow points to its location in original scan). In addition, the right fat DTI cannot be seen in this same slice as it is higher than original scan (a), but medical notes indicate this right abnormality (hematoma) is still present. This corresponds to the ultrasound image (c) using a 4–7 MHz linear probe with musculoskeletal presets that demonstrates a hypoechoic area consistent with a hematoma overlying the right IT in the subcutaneous (fat) layer (arrow) overlying the lowest point of the right IT. It was estimated to be 8 × 15 × 18 mm. (d) Peak interface pressures were ≥200 mm Hg under right IT and 161 mm Hg under the left IT in loaded sitting on the patient's own wheelchair cushion (left image) with concurrent high pressure gradients for both IT regions with right greater than left (right image). The right fat DTI corresponds to the high right peak pressure and high right pressure gradient.
(a) Case 3: CT scan on admission demonstrates a large (170 × 71 mm) recent hematoma in the gluteus medius of the left buttocks (arrowhead). On the right, there is a subcutaneous (fat) deep tissue injury (DTI; box). The arrow is positioned at the most medial extent of the gluteus maximus muscle; everything medial to it is the fat DTI. (b) The CT scan 1 month later is captured at a higher level than the original scan (a); however, medical notes indicate a decrease in the size of the left hematoma in the gluteus medius (arrow points to its location in original scan). In addition, the right fat DTI cannot be seen in this same slice as it is higher than original scan (a), but medical notes indicate this right abnormality (hematoma) is still present. This corresponds to the ultrasound image (c) using a 4–7 MHz linear probe with musculoskeletal presets that demonstrates a hypoechoic area consistent with a hematoma overlying the right IT in the subcutaneous (fat) layer (arrow) overlying the lowest point of the right IT. It was estimated to be 8 × 15 × 18 mm. (d) Peak interface pressures were ≥200 mm Hg under right IT and 161 mm Hg under the left IT in loaded sitting on the patient's own wheelchair cushion (left image) with concurrent high pressure gradients for both IT regions with right greater than left (right image). The right fat DTI corresponds to the high right peak pressure and high right pressure gradient.
Discussion
The aim of this article was to describe the utility of ultrasound in 3 cases of DTI in persons with SCI, specifically the abnormal signs, location in the soft tissue layers overlying the IT, and the importance of medical histories in establishing the imaging diagnosis. Ultrasound detected 5 DTIs in 2 males (AIS A) and 1 female (AIS B) with SCI who were hospitalized for 1 to 3 months, which included bed rest.
There were a variety of abnormal ultrasound signs, which included a hypoechoic pseudo capsule, a complex cystic collection, heterogeneous echotexture, hyperechogenicity, a hypoechoic area, and areas of anechoic (fluid) and solid/soft tissue echotexture. To our knowledge, a pseudo capsule, complex cystic collection, hyperechogenicity, and areas of anechoic (fluid) are new signs for ultrasound-detected DTI and, in particular, in persons with SCI.2,6–8,18 There is a need for a standardized ultrasound protocol, including an abnormal tissue report, to describe the full spectrum of ultrasound signs in the layers overlying this bony prominence.
The lowest point of the IT is the region of the pelvis that loads the soft tissues during sitting.19,20 Four soft tissue layers and the ischial-gluteal bursa overly this bony prominence: hamstring muscle complex (biceps femoris, semitendinosus, and semimembranosus muscles), gluteus maximus muscle, subcutaneous fat, and skin.21,22 The conjoint tendon of biceps femoris and semitendinosus is commonly seen on ultrasound in the longitudinal view.22 DTI is thought to typically originate in deep tissues such as the gluteus muscle near bony prominences, and this can correspond to the highest strains in the deep tissues as demonstrated by finite element model analysis13,20,23; however, the DTIs in the current study were detected in the fat and muscles overlying or adjacent to the IT. In addition, individuals with AIS A complete SCI can have absent skeletal muscles,24 but one patient with AIS A in the present study had a gluteal muscle layer and the other patient was indeterminate on ultrasound.
The histories of these 3 cases included a stage 1 PI due to excessive loading and shear during 3 to 5 hours of frequent hand cycling on a rigid surface, infection (cellulitis) in the groin and buttocks region, and hematomas secondary to anticoagulant treatment. In 2 cases, excessive interface pressures confirmed that the compression of buttocks soft tissues likely exceeded tissue tolerance thresholds and DTIs developed.25–27 None of these ultrasound-detected DTIs progressed to open wounds during hospitalization with the interventions described. In one case, the ultrasound and interface pressure mapping images served as a behavior change technique to motivate the patient to purchase a new cushion for his hand cycle and enhance his skin inspection regimen. Fogelberg and colleagues reported that the development of PIs were associated with the individual's wheelchair and/or cushion selection/adjustment, lifestyle choices, and challenging life contexts,28 thereby emphasizing the need for patients to self-manage using information such as their own ultrasound and pressure mapping images.
The differential diagnosis of abnormal tissue overlying the ischium includes ischial-gluteal bursitis, trauma, neoplasia, hematoma, and infection.29,30 These are essential to assess as imaging diagnoses are made in the context of medical history.31,32 The 3 cases presented illustrate the need to use imaging such as CT and ultrasound to monitor changes in the DTIs and diagnose the development of additional lesions in this high-risk anatomical area and patient population.
This study was limited to 3 adults with SCI with ultrasound-detected DTIs, but these data have informed the development of a standardized ultrasound protocol for detecting, measuring, and describing abnormal signs in the soft tissues overlying the IT. The routine use of real-time ultrasound for screening high-risk areas such as the IT and sacrum has been advocated2 and conducted in high-risk groups such as elite athletes,7,8 but it is not part of routine practice within SCI services internationally. Visualization of abnormal tissue may be a key behavioral change motivator for individuals33 to increase their participation in prevention routines and equipment choices while simultaneously providing requisite evidence for insurance companies to fund these services. Knowledge translation and implementation will be required to develop an evidence-based clinical pathway for these ultrasound-detected DTIs in persons with SCI, thus requiring an interdisciplinary team, including musculoskeletal radiology.34
These case studies have highlighted the need for a prospective study to determine whether early detection of an ultrasound-detected DTI in persons with SCI is associated with the development of a PI. Presently, the AusCAN Risk Scale Study for Sitting-Acquired Pressure Ulcers has obtained some of those data by using a standardized real-time ultrasound protocol, and the results are presently being analyzed. This current study of 3 case studies demonstrates the utility of ultrasound for diagnosing DTIs in individuals with SCI, for safely monitoring these DTIs over time, and for motivating self-management behaviors, such as choosing to use an optimal wheelchair cushion and enhancing a skin inspection regimen.
Acknowledgments
Rosemary L'Angat and Marilyn Zelesco are the senior sonographers who assisted with the design of the protocol and performing the sonography assessments. Vi Tran and Marianne Mullane are occupational therapists and research assistants who assisted in acquiring the ultrasound images and interface pressure maps. Dr. Mohammad Khan assisted with the medical chart review.
This research was supported by the Fremantle Hospital Medical Research Foundation, the Australian Wound Management Foundation, and the National Health and Medical Research Council (grant #634388). Ms. Swaine was funded by the University of Western Australia/Warren Jones Postgraduate scholarship for her doctorate. The authors declare no other conflicts of interest.
Ethical approval was obtained from Human Research Ethics Committees at the hospital and university (SMAHS #9/326 and SMAHS #9/414). All participants signed informed consent, all data were de-identified, and confidentiality was assured. The CARE guidelines, consensus-based clinical case report guideline development, were followed for this report.
