References

Shafipour V, Ramezanpour E, Gorji MA, Moosazadeh M. Prevalence of post-operative pressure ulcer: A systematic review and meta-analysis. Electron Physician. 2016; 8:(11)3170-3176 https://doi.org/10.19082%2F3170

Sato M, Konya C, Murayama S Wound healing process in Stage I pressure ulcers – Based on 14 patients. Jpn J PU. 2004; 6:(1)63-67

Minematsu T, Nakagami G, Yamamoto Y Wound blotting: a convenient biochemical assessment tool for protein components in exudate of chronic wounds. Wound Repair Regen. 2013; 21:(2)329-334 https://doi.org/10.1111/wrr.12017

Asada M, Nakagami G, Minematsu T Novel biomarkers for the detection of wound infection by wound fluid RT-PCR in rats. Exp Dermatol. 2012; 21:(2)118-122 https://doi.org/10.1111/j.1600-0625.2011.01404.x

Nakagami G, Sanada H, Iizaka S Predicting delayed pressure ulcer healing using thermography: a prospective cohort study. J Wound Care. 2010; 19:(11)465-6 https://doi.org/10.12968/jowc.2010.19.11.79695

Kanazawa T, Kitamura A, Nakagami G Lower temperature at the wound edge detected by thermography predicts undermining development in pressure ulcers: a pilot study. Int Wound J. 2016; 13:(4)454-460 https://doi.org/10.1111/iwj.12454

Ueta M, Sugama J, Konya C. Use of ultrasound in assessment of necrotic tissue in pressure ulcers with adjacent undermining. J Wound Care. 2011; 20:(11)503-510 https://doi.org/10.12968/jowc.2011.20.11.503

Yabunaka K, Nakagami G, Kitamura A Visualization of blood flow in an undermined pressure ulcer revealed by sonographic imaging and clutter suppression post-processing: a case report. J Diag Med Sonogr. 2016;

Aoi N, Yoshimura K, Kadono T Ultrasound assessment of deep tissue injury in pressure ulcers: Possible prediction of pressure ulcer progression. Plast Reconstr Surg. 2009; 124:(2)540-550 https://doi.org/10.1097/PRS.0b013e3181addb33

Yabunaka K, Iizaka S, Nakagami G Can ultrasonographic evaluation of subcutaneous fat predict pressure ulceration?. J Wound Care. 2009; 18:(8)192-198 https://doi.org/10.12968/jowc.2009.18.5.42173

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Changes of tissue images visualised by ultrasonography in the process of pressure ulcer occurrence

01 April 2019

Abstract

Objective:

Ultrasonography is suitable for assessing pressure ulcers, and several features of ultrasonographic images that indicate abnormalities have been reported. However, no study has compared ultrasonographic images between normal and pressure-loaded skin and subcutaneous tissue from the same patients. This study aimed to assess lateral thoracic tissue using ultrasonography for both pre- and postoperative conditions and investigate changes in the tissue caused by loading. Surgeries were performed with patients in the park-bench position.

Method:

A nursing researcher obtained ultrasonographic images of the skin and subcutaneous tissue of the lower thoracic region in areas in contact with the surgical table one or two days before and after surgery. This study focused on three groups of two patients who had a category I pressure ulcer (PU), blanchable erythema, or normal skin on their lateral thoracic region.

Results:

A total of six patients participated. Postoperatively, muscle layers became thinner and less clear compared with pre-operative conditions in patients with the Category I pressure ulcers. These patients complained of significant pain in the areas of their pressure ulcers.

Conclusion:

Thickness of muscle layers could be an early sign of deep tissue injury.

Prevalence of postoperative pressure ulcers (PU) (also called pressure injuries) has been reported to be 19%.1 High numbers of postoperative PUs suggest that both preventing PU development and shortening wound healing time by an accurate assessment of the wound pathophysiology are important. Category I PUs are more common than other postoperative injuries.1 A prospective study that followed the healing process of category I PUs reported that four out of 15 PUs deteriorated to category II.2 Understanding the extent of tissue damage at the onset of pressure loading is needed to provide optimal PU management to prevent PU deterioration.

Several methods using wound fluid have been used for PU assessment.34 However, these methods cannot be used for the category I PU because the skin remains intact. Methods that visualise changes in internal structures, such as thermography and ultrasonography, have been used in clinical settings.5,6,78 In particular, ultrasonography is suitable for observation of superficial to deep tissue structures. Ultrasonography visualises tissue structures using ultrasound waves that reflect at the boundaries between tissues of different density. Previous studies reported that abnormal features in ultrasonographic images of PUs may predict wound prognosis, including deterioration of deep tissue injury (DTI).910 A limitation of previous studies using ultrasonographic assessment is that abnormal features reported only images collected after tissue damage had occurred. These studies may have missed some changes in tissue that accompany PUs. Furthermore, although Helvig and Nichols reported abnormal ultrasonographic images of both visible and internal heel PUs,11 the heel anatomy is not representative of other sites due to lack of muscle layers. This study aimed to assess lateral thoracic tissue using ultrasonography among patients who underwent surgery in the park-bench position12 for both pre- and postoperative conditions, and investigate changes in the tissue caused by loading.

Materials and methods

This study was a secondary analysis of data collected for the study which investigated risk factors for the development of intraoperatively acquired PUs in the park-bench position,13 a specific position for neurosurgery (Fig 1). The incidence of park-bench position-related PUs has been reported to be 14–48%.1415 We collected data between April and November 2014 from an operating room in a general hospital in Japan. This hospital provided preventive care, such as the use of foam mattresses on operating beds and changing patients' positions, to minimise intraoperatively-acquired PUs based on the guidelines of the Japanese Society of Pressure Ulcers. The study protocol was approved by the Ethics Committee of the Graduate School of Medicine, the University of Tokyo. The individuals assessed in this manuscript have given written informed consent to publish these case details. The study complied with the Declaration of Helsinki.

Fig 1. Park-bench position

Patients in the study had no skin disease or symptoms on their lateral thoracic region before the surgery. A nursing investigator obtained ultrasonographic images of skin and subcutaneous tissue on the vertical axis in the lower thoracic region (on the axillary line from 5th to 10th ribs), an area in contact with the surgical table in the park-bench position, one or two days before and after the surgery. Participants kept the same position, with their shoulder joint at 90 degrees of abduction and elbow joint at 90 degrees of flexion during ultrasonographic examination. B-mode images were obtained using SonoSite M-Turbo and 6-15 MHz linear probe (Fujifilm, Tokyo, Japan) within a few minutes. Nurses observed patients' skin after surgery to determine whether PUs occurred.

This study focused on patients divided into three groups, namely category I PU (non-blanchable erythema), blanchable erythema, and normal skin on their lateral thoracic region.16 Patients' demographic and intraoperative data collected from their medical records are shown in Table 1. All patients underwent intracranial tumorectomy in the park-bench position. No relationship was apparent between patient demographic data and the occurrence of PU.


Table 1. Patient demographic and intraoperative data
Case 1 2 3 4 5 6
Pressure ulcer status Category I Category I Blanchable erythema Blanchable erythema Intact skin Intact skin
Demographic data
Age (years) 50 36 50 45 63 68
Sex (male/female) M M F M F F
Body mass index (kg/m2) 22.0 20.4 22.4 26.5 19.9 24.1
Braden Scale score 23 23 22 23 23 23
ASA* physical status classification 2 1 1 1 1 2
Intraoperative data
Length of surgery (hours) 8.1 9.5 8.0 5.7 7.2 5.5
Use of rotation No No Yes Yes Yes No
* ASA—American Society of Anesthesiologists

Results

A total of six patients participated in the study. A category I PU, non-blanchable erythema, occurred in two cases. Sizes (major axis × minor axis) of injuries were 14×7cm and 10×3.5cm for cases 1 and 2, respectively. PUs were located around the 6th and 7th ribs in case 1 and on the 5th and 6th ribs in case 2. Ultrasonographic images obtained of the 6th rib demonstrated that muscle layers became thinner and unclear (hyperechoic lines of muscle layers disappeared or weakened) postoperatively compared with those pre-operatively (Fig 2a, 2b, 2d, and 2e). Locations, where muscle layers thinned, were consistent with locations of PUs. An unclear layer of subcutaneous fat, indicating oedema, was observed regardless of the presence of a PU (Fig 2q). This layer was most evident for blanchable erythema cases (Fig 2h and 2k). Table 2 summarises changes in ultrasonographic images. Furthermore, the subcutaneous fat layers were thicker before surgery for blanchable erythema cases. Patients with category I PUs complained of pain at the area of ulcers for about 10 days, indicating DTI. Category I PUs healed 10 and 19 days after their surgeries in cases 1 and 2, respectively.

Fig 2. Pre- and postoperative ultrasonographic images. Ultrasonographic images of pre- and postoperative and photographs of the skin of 6 cases (Case 1 to 6) are shown. Images in the left are preoperative ultrasonographic images, those in the center are postoperative. Brightness of the ultrasonographic images is adjusted in this figure. C and F are category I pressure ulcer. I and L are blanchable erythema. O and R are skin without erythema. Yellow two-way arrows show thinner and unclear muscle layers postoperatively compared with those of preoperative. Red two-way arrows show the thicker fat layer that indicates subcutaneous oedema. A black arrow in each photograph indicates direction of the patient's head

Table 2. Changes of the ultrasonographic images detected after the surgery
Case 1 2 3 4 5 6
Location Feature Category I Category I Blanchable erythema Blanchable erythema Intact skin Intact skin
Muscle layer Thinner + +
Fat layer Unclear layer (oedema) + + + + +
Fat layer Thicker + + +

Discussion

This study revealed changes in tissue visualised by ultrasonography before and after the occurrence of intraoperative PU. We assessed ultrasonographic images of category I PUs and identified thinner and less clear muscle layers than those observed in cases of blanchable erythema or normal skin.

Sato et al. reported that indicators of the deterioration of category I PU were locations other than a bony prominence and darker red erythematic areas.2 However, they included only PUs in the sacral and coccygeal regions. These indicators cannot be for the thoracic region, which is a pressure-loading area for the park-bench position, because of differences in anatomical structures, that is, the ribs. Also, Helvig and Nichols reported heel PUs detected as abnormalities (dark areas) in ultrasonographic images. However, heels are covered by a fat pad.17 This study, therefore, investigated changes in the tissue using ultrasonography to find a new and more general predictor of deterioration of category I PU focusing on muscle and fat layers.

In the previous study, four types of ultrasonographic features are reported as abnormal signs of deep tissue damage: (1) unclear layered structure, indicating oedema; (2) hypoechoic lesion, indicating a lesion with fluid such as seroma and haematoma; (3) discontinuous deep fascia, indicating damage of muscle; and (4) heterogeneous hypoechoic area, indicating a necrotic area containing necrotic tissue, debris, and fluid.9 In this study, three of these signs (hypoechoic lesion, discontinuous fascia, and heterogeneous hypoechoic area) were not observed. In the previous study,9 most PUs with discontinuous fascia or heterogeneous hypoechoic areas deteriorated to category III/IV, although category I PUs in this study did not ulcerate. This result supports the interpretation described in the previous study that discontinuous fascia and heterogeneous hypoechoic areas could be indicators of severe deep tissue damage.9 Meanwhile, less clear layer structure, indicating subcutaneous oedema, was observed, regardless of the presence of a PU. Lack of clarity was not striking and hyperechoic lines were visible in the fat layers of blanchable erythema in the present study. Fat layers did show expansion. A possible reason that ultrasonographic images of oedema showed different appearances for fat layers in the previous study is that differences in clarity and expansion of fat layers correlate with the severity of oedema. Thinning of muscle layers, a new finding in this study, could be an early sign of DTI. A park-bench position causes high interface pressure in the lower thoracic region due to a small contact area. The thickness of muscle layers could demonstrate deformation of muscle layers by pressure loading.

It is unknown how long changes in muscle layers persist after surgery (pressure release). Furthermore, category I PUs in this study caused persistent, substantial pain. We did not follow patients until complete healing in this study. Further research is needed to investigate the course of healing of pressure injuries using ultrasonography.

Limitations

A limitation of this study is that only the thoracic region was observed because PUs frequently occur in this area in the park-bench position. Further investigation is required to confirm whether the changes in the tissue found in this study can be generalised to other body parts when PUs occur.

Conclusion

This study demonstrated thinning and lack of clarity of muscle layers in ultrasonographic images from category I PUs just after PU occurrence. Earlier detection of PUs by ultrasonography would enable health professionals to provide care to enhance healing. Vibration therapy is reported to enhance healing of PUs due to enhancement of blood flow,18 and the use of ultrasonography might indicate the most appropriate time for such therapy.

Reflective

  • How can ultrasonography be used for assessment of pressure ulcers?
  • Is oedema, indicated by unclear layered structure and thicker fat layer, observed in the region with blanchable erythema?
  • Can thinning and lack of clarity of muscle layers indicate damage of deep tissue?