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Original Research
Pathogenetic Mechanisms and Classification of Undermining in Pressure Ulcers—Elucidation of Relationship with Deep Tissue Injury
Schultz et al1 reviewed wound bed preparation and undermining in patients with pressure ulcers and proposed a new term “edge of nonadvancing.” They demonstrated and warned that undermining in pressure ulcers differs from other ulcer types regarding the healing process. Cases of undermining in pressure ulcers are far more intractable than those without undermining. Nevertheless, the authors’ extensive literature search revealed no systematic studies on the mechanisms and classification of undermining in cases of pressure ulcers.2-6
Deep tissue injury (DTI) has recently become an unexpectedly spotlighted issue in the United States because these wounds are difficult to heal and are likely to exacerbate. There has been much discussion regarding which categories of DTIs should be placed under the National Pressure Ulcer Advisory Panel (NPUAP) classification.7-11
The present study analyzed Stage III and IV pressure ulcers and cases of so-called DTI pressure ulcers that were treated and followed from the onset throughout. This study describes the results of interest from the study demonstrating the cause of development and clinical progress of undermining arising from deep pressure ulcers.
h3>Necrotized Tissue Morphology in Deep Pressure Ulcers Deep pressure ulcers and undermining in pressure ulcers were examined during the necrosis phase using CT scans and ultrasonography, morphologic characterization of necrosis, and follow-up for clinical progress.
Morphologic observation of the time-course of necrosis in cross sections of decubitus ulcers has led to classification of necrosis into 2 patterns. The patterns of necrosis are shown in cross sections (Figures 1 and 2). The cross section of the necrotic lesion assumes a rectangular shape in cases of relatively shallow pressure ulcers and occasionally will in cases of deep pressure ulcers. Even if a necrotic lesion like this undergoes histolysis and subsequent discharge, it merely forms an ulcer and does not lead to undermining.
In cases of deep pressure ulcers, tissues adjacent to a bony prominence are likely to be extensive and severe due to the impact of mechanical stress. Consequently, the cross section of the lesion reveals an hourglass-shaped contour of necrosis. After histolysis and discharge occurs, a cavity under the intact skin remains and can be viewed from the surface (undermining). Although several factors are involved in the development of hourglass-shaped necrosis, a clear explanation of the phenomenon is not fully understood. Despite lack of explanation, it is imperative to further discuss the clinical relevance of such cases.
Time to histolysis and discharge. Histolysis and discharge of necrotized tissues are inconsistent depending on the thickness and volume of the necrotic tissue, degree of bacterial infection, and moist state of the lesion or therapies given. The duration of liquefaction/discharge of necrotic tissue varies widely. Surgical or sharp debridement of a necrotic lesion has a direct and substantial effect on histolysis/discharge and may hasten discharge of necrotized tissues.1 Wounds that present with dry, thick necrotic tissue that are sharp of surgically debrided show more rapid liquefaction of the residual necrotic tissue. Surgical of sharp debridement may thereby hasten necrotic tissue discharge.
Sequential undermining. Discharge undermining precedes sequential undermining, which subsequently shifts to the external type due to external forces during healing of the discharge type ulcer. Eventually, there are changes in size and shape of undermining from the initial state; direction of the undermining is toward a bony prominence from the wound margins, hence a localized undermining biased in size and shape.
Newly onset undermining. This is an external force undermining that occurs within the pressure ulcer and is not preceded by discharge undermining. It occurs because some external force has been applied to the ulcer and develops at the time of granulation tissue growth or when necrotic tissue has mostly disappeared.
Etiology. Development of this type of undermining is consequent on an intricate complex of soft tissue movement to a bony prominence and compression (Figure 4). A probable pathogenetic mechanism of the undermining is soft tissue movement toward the bony prominence caused by various external forces and complex stress that is superimposed on it. A typical case of a pressure ulcer and undermining development is presented (Figure 5 and 6). It is advisable to manually move the existing pressure ulcers and undermining along with the surrounding soft tissues. Moving the existing ulcers assists in finding the cause and direction of shearing with this type of undermining. To determine the external force load, it is advisable to manually shift the soft tissue with the undermining cavity over the bony prominence. The soft tissue should easily move in the direction of the bony prominence and reveal the direction of the tangential forces that are loaded during positioning that create the external forces that cause undermining (Figure 7).
Morphological characteristics. External force undermining frequently exists in a limited direction, typically toward the bony prominence site. The wound margin facing the undermining is freed from the wound bed while the wound margins not facing the undermining adhere closely to the wound bed and show epithelial growth over the ulcer surface. Such manifestations indicative of healing tendency are inconspicuous along the wound margins with discharge undermining.
Treatment and pressure relief mattress. All patients were provided with a pressure relief mattress appropriate in consideration of risk factors of pressure ulcer in Japanese subjects and according to wound status. The pressure ulcer risk factor level for Japanese subjects, the probability of onset (%), the healing period, and total scores were tabulated (Table 1).12-13
The wounds were cleansed with saline solution and a dressing was applied over the wound to maintain moisture. The dressing was changed daily or once every 2 days, depending on the amount of exudate that was present. Liquefied necrotic tissues were removed as often as possible using scissors and scalpel.
Treatment duration assessment. Of the 99 cases, 52 patients were excluded–death (35); moved to other hospital (7); ulcer located in another region (10). They were excluded because the approximate mean duration of 150 days typically elapses until shifting to the external force type, so that exploration for a cut-off point resulted in the conclusion that 360 days after onset would be appropriate. A total of 47 patients were assessed.
Group 1: Patients who had discharge undermining ulcers throughout the healing process that did not develop external force undermining.
Group 2a: Patients in whom undermining occurred and, after a subsequent while (4-32 weeks), the lesion shifted to an external force type.
Group 2b: Patients in whom there was no undermining initially, followed by development of an external force type undermining.
The duration of the healing process in each group was assessed comparatively. First, the duration of the healing process in Group 1 patients whose ulcers healed was compared to healing in Group 2a and Group 2b patients. Second, the duration of the healing process in Group 1 patients was compared to Group 2a and Group 2b patients. All pair-wise mean comparisons among groups were calculated using Tukey’s HSD test.
The differences in comparative healing times between groups are shown in Figure 9. Significant differences were also noted between Group 1 and Group 2a, and between Group 1 and Group 2b (Figure 10).
Case 2. A man, age 73 years with subarachnoid hemorrhage, dementia, and pressure ulcers (Stage IV) in sacral region (Figure 12). The patient’s risk factor score was 8.5 (self-sustainability, impossible = 3; morbid bony prominence = 1.5; articular contracture = 1; edema = 3). The patient had severe level risk factors. The general condition of the patient improved to a total score of 4 (edema, 0; and self-sustainability, intermediate, 1.5).
The ADVAN (high performance type air mattress) pressure relief mattress was used. Discharge type undermining shifted to sequential undermining of the external force type.
Ultrasonography showed a highly dense area of necrotic tissue in the subcutaneous layer.
Morphologic observation of the time-course of necrosis in cross sections of decubitus ulcers has led to classification of necrosis into 2 patterns. The patterns of necrosis are shown in cross sections (Figures 1 and 2). The cross section of the necrotic lesion assumes a rectangular shape in cases of relatively shallow pressure ulcers and occasionally will in cases of deep pressure ulcers. Even if a necrotic lesion like this undergoes histolysis and subsequent discharge, it merely forms an ulcer and does not lead to undermining.
In cases of deep pressure ulcers, tissues adjacent to a bony prominence are likely to be extensive and severe due to the impact of mechanical stress. Consequently, the cross section of the lesion reveals an hourglass-shaped contour of necrosis. After histolysis and discharge occurs, a cavity under the intact skin remains and can be viewed from the surface (undermining). Although several factors are involved in the development of hourglass-shaped necrosis, a clear explanation of the phenomenon is not fully understood. Despite lack of explanation, it is imperative to further discuss the clinical relevance of such cases.
Time to histolysis and discharge. Histolysis and discharge of necrotized tissues are inconsistent depending on the thickness and volume of the necrotic tissue, degree of bacterial infection, and moist state of the lesion or therapies given. The duration of liquefaction/discharge of necrotic tissue varies widely. Surgical or sharp debridement of a necrotic lesion has a direct and substantial effect on histolysis/discharge and may hasten discharge of necrotized tissues.1 Wounds that present with dry, thick necrotic tissue that are sharp of surgically debrided show more rapid liquefaction of the residual necrotic tissue. Surgical of sharp debridement may thereby hasten necrotic tissue discharge.
Classification and Definition of Undermining in Pressure Ulcers
Undermining can be classified into 2 categories according to etiology and morphology–discharge type: liquefied necrosis discharge (initial phase); and external force type (late phase). Figure 3 shows the scheme of classification, cause, and process of undermining. The external force category is further broken down into 2 types, depending on whether the injury was preceded by discharge undermining (ie, sequential undermining of external force and newly onset undermining of external force).Discharge Undermining
Time course. Undermining of this type arises in the initial phase of the pressure ulcer healing process. Etiology. Pressure ulcers arise from disturbance of local blood flow (ischemia) due to a complex involvement of pressure and shear force. Particularly in Stage III and IV pressure ulcers, deep, soft tissues in the vicinity of a bony prominence can become necrotized extensively and severely. Cross sections of these ulcers viewed with a CT scan or ultrasonography reveal hourglass-shaped necrosis. As this ulcer remains a cavity after histolysis and discharge of the necrotic tissue, undermining forms beneath the healthy skin layer when viewed from the surface. Morphological characteristics. Margins of an undermining site are freed along almost the entire circumference of wound bed, and in most instances, the undermining extends as a concentric cavity under the intact skin from the wound surface.External Force Undermining
Time course. This type of undermining develops in the middle or late phase of pressure ulcer healing. Undermining of external force type is classified into two as follows.
Sequential undermining. Discharge undermining precedes sequential undermining, which subsequently shifts to the external type due to external forces during healing of the discharge type ulcer. Eventually, there are changes in size and shape of undermining from the initial state; direction of the undermining is toward a bony prominence from the wound margins, hence a localized undermining biased in size and shape.
Newly onset undermining. This is an external force undermining that occurs within the pressure ulcer and is not preceded by discharge undermining. It occurs because some external force has been applied to the ulcer and develops at the time of granulation tissue growth or when necrotic tissue has mostly disappeared.
Etiology. Development of this type of undermining is consequent on an intricate complex of soft tissue movement to a bony prominence and compression (Figure 4). A probable pathogenetic mechanism of the undermining is soft tissue movement toward the bony prominence caused by various external forces and complex stress that is superimposed on it. A typical case of a pressure ulcer and undermining development is presented (Figure 5 and 6). It is advisable to manually move the existing pressure ulcers and undermining along with the surrounding soft tissues. Moving the existing ulcers assists in finding the cause and direction of shearing with this type of undermining. To determine the external force load, it is advisable to manually shift the soft tissue with the undermining cavity over the bony prominence. The soft tissue should easily move in the direction of the bony prominence and reveal the direction of the tangential forces that are loaded during positioning that create the external forces that cause undermining (Figure 7).
Morphological characteristics. External force undermining frequently exists in a limited direction, typically toward the bony prominence site. The wound margin facing the undermining is freed from the wound bed while the wound margins not facing the undermining adhere closely to the wound bed and show epithelial growth over the ulcer surface. Such manifestations indicative of healing tendency are inconspicuous along the wound margins with discharge undermining.
Methods
Patients. The study population comprised 593 patients with Stage III or IV pressure ulcers (as defined by the National Pressure Ulcer Advisory Panel [NPUAP]) who were treated by the authors until ulcer healing occurred in the 4-year period from 2002 to 20059,10 (Figure 8). Of these patients, those who died within 4 weeks after pressure ulcer onset and those who moved to other hospitals were excluded. Only those patients whose general condition and local status were relatively stable and those who had overcome an unstable acute healing stage were selected, because general and local conditions fluctuate noticeably about 4 weeks after pressure ulcer onset. The authors reasoning was that patients who died within 4 weeks after pressure ulcer onset frequently have high fever, are generally unstable, and could not be offloaded from pressure or shear force. Secondly, there were no cases in which deep pressure ulcers developed undermining within 4 weeks without surgical debridement.
Treatment and pressure relief mattress. All patients were provided with a pressure relief mattress appropriate in consideration of risk factors of pressure ulcer in Japanese subjects and according to wound status. The pressure ulcer risk factor level for Japanese subjects, the probability of onset (%), the healing period, and total scores were tabulated (Table 1).12-13
The wounds were cleansed with saline solution and a dressing was applied over the wound to maintain moisture. The dressing was changed daily or once every 2 days, depending on the amount of exudate that was present. Liquefied necrotic tissues were removed as often as possible using scissors and scalpel.
Treatment duration assessment. Of the 99 cases, 52 patients were excluded–death (35); moved to other hospital (7); ulcer located in another region (10). They were excluded because the approximate mean duration of 150 days typically elapses until shifting to the external force type, so that exploration for a cut-off point resulted in the conclusion that 360 days after onset would be appropriate. A total of 47 patients were assessed.
Group 1: Patients who had discharge undermining ulcers throughout the healing process that did not develop external force undermining.
Group 2a: Patients in whom undermining occurred and, after a subsequent while (4-32 weeks), the lesion shifted to an external force type.
Group 2b: Patients in whom there was no undermining initially, followed by development of an external force type undermining.
The duration of the healing process in each group was assessed comparatively. First, the duration of the healing process in Group 1 patients whose ulcers healed was compared to healing in Group 2a and Group 2b patients. Second, the duration of the healing process in Group 1 patients was compared to Group 2a and Group 2b patients. All pair-wise mean comparisons among groups were calculated using Tukey’s HSD test.
Results
Frequency of undermining types is shown in Figure 8. There were 593 patients with Stage III or IV pressure ulcers treated during the 4-year period. From this group, 560 patients were analyzed excluding 33 patients who died or moved to other hospitals. Of the 560 patients with a deep decubitus ulcer, 99 showed evidence of undermining–about 17.7% of patients with deep pressure ulcers. Pressure ulcers were located in the sacral region in 66 patients, the trochanter major region in 19 patients, ischial region in 4 patients), and other regions (eg, hand, upper arm, lower limb) in 10 patients. Duration of the healing process in patients with pressure ulcer undermining who survived and were treated in the same hospital(s) for ≥ 360 days after pressure ulcer onset were assessed comparatively, excluding the 10 patients whose ulcers were located in other regions (eg, lower limb, heel, hand, fingers). Discharge of liquefied necrosis type (Group 1) was found in 13 cases. The average healing time duration was 148.6 days (± 18.9). The discharge of liquefied necrosis that shifted and changed to external force type (Group 2a) was found in 34 cases. The average healing time was 311.8 days (± 26.7). Newly onset undermining of external force (Group 2b) was found in 8 cases. The average healing time duration was 274.4 days (± 70.5).
The differences in comparative healing times between groups are shown in Figure 9. Significant differences were also noted between Group 1 and Group 2a, and between Group 1 and Group 2b (Figure 10).
Case Reports
Case 1. A woman, age 76 years with cerebral infarction and pressure ulcers in sacral region (Figure 11). The ulcer had discharge type undermining and the patient’s risk factor score was 6 (self-sustainability, impossible = 3; morbid bony prominence = 3). The patient had middle level risk factors. The mattress used was ADVAN (air mattress, 15 cm thickness). CT scans were taken prior to discharge of necrotic tissues to examine the lower tissue layer of decubitus ulcer, especially the condition in the vicinity of the bony prominence. Necrotic tissue is shown at high-density area in the subcutaneous layer.
Case 2. A man, age 73 years with subarachnoid hemorrhage, dementia, and pressure ulcers (Stage IV) in sacral region (Figure 12). The patient’s risk factor score was 8.5 (self-sustainability, impossible = 3; morbid bony prominence = 1.5; articular contracture = 1; edema = 3). The patient had severe level risk factors. The general condition of the patient improved to a total score of 4 (edema, 0; and self-sustainability, intermediate, 1.5).
The ADVAN (high performance type air mattress) pressure relief mattress was used. Discharge type undermining shifted to sequential undermining of the external force type.
Ultrasonography showed a highly dense area of necrotic tissue in the subcutaneous layer.
Discussion
Recently, DTI-related issues have been spotlighted,7-11 but research that investigates the etiology of DTI is limited. The DTI under intact skin is undoubtedly hourglass-shaped necrosis and represents undermining subsequent to histolysis and discharge of that tissue.10 Le et al14 demonstrated in their study of deep pressure ulcers using a meat model that a region proximate to bone is markedly and extensively compressed. Gefen et al15 reported that muscles in the vicinity of bone became stiff in the early stage of pressure application in experiments using rat models and finite element analysis. Undermining occurs in ulcers of other etiologies as well. Undermining that develops in pressure ulcers, unlike that in other chronic ulcers, is thought to have a more profound bearing on external forces and intra-tissue stress, and the authors believe should be considered separately from undermining in other chronic ulcers. In the present study, 560 patients with Stage III to IV deep pressure ulcers were analyzed. There were 99 patients (17.7%) who had an undermining. This incidence of undermining is considered to be lower compared to other hospitals in Japan12 because the hospitals with which the present authors are affiliated have a relatively high-level nursing staff and provide care with particular attention to occurrence and prevention of pressure and shearing regarding patient re-positioning. It is surprising that as many as 17.7% of Stage III and IV pressure ulcers developed hourglass-shaped necrosis due to undermining. Further investigation is necessary to determine how the undermining progresses and which factors influence it most. It is clinically important to classify and distinguish undermining type because undermining of the discharge type cannot be prevented, whereas undermining of the external force type is preventable. The discharge type represents a DTI where hourglass-shaped necrotic tissue liquefies and creates a cavity and remains as undermining when viewed from the overlying intact skin. Therefore, the extent and severity of undermining of this type are mostly determined according to the severity and extent of underlying ischemia that causes pressure ulcers to develop. This process is shown in Figure 11. Underlying ischemia can be confirmed in the necrotized tissue even at an initial stage by CT scans and ultrasonography imaging. It thus follows that the ensuing chain of events consisting of necrosis, histolysis, discharge, and undermining formation constitutes a natural healing process, so that the development of a discharge type undermining cannot be prevented by the nursing care provided after the development of pressure ulcers. External force undermining arises from a complex process comprising soft tissue movement toward a bony prominence and mechanical stress in the course of pressure ulcer treatment. It is important to eliminate external forces to prevent external force undermining. Prevention of external force undermining is preventable through meticulous nursing care. In cases where external force undermining has developed, time to healing would be prolonged and it would be difficult to attain healing unless nursing care is able to eliminate pressure and shearing. Ultrasonography, CT scanning, and MRI are useful for early detection of subcutaneous necrotic tissues. Therefore, the patient should be screened to establish a definitive diagnosis regarding the depth and extent of the wound to delineate the prognosis or to prevent complaints (mostly from family members, sometimes patients or attendants) that the pressure ulcers were aggravated due to qualitatively inadequate nursing care. Caution must be exercised for a wound in the ischiatic region, which has a thick layer of soft tissues where the wound does not go through a typical undermining process, unlike wounds in the sacral and greater trochanter regions. Healing times of pressure ulcers with undermining between the 2 ulcer types were comparatively assessed. As a result, a significant difference was found in the duration between the discharge type and the external force type, indicating that undermining of the external force type is difficult to cure because it is formed subsequent to application of external force. Furthermore, the 2 subtypes of external force undermining also showed significant differences from the discharge undermining in terms of healing time. This stresses the importance of preventing the development of external force undermining through nursing care because once developed, healing is substantially delayed compared to discharge undermining. Once external force undermining has developed, the external forces causing the undermining must be eliminated before instituting treatment.Conclusion
Undermining in pressure ulcers can be classified into 2 types according to the underlying pathogenetic mechanisms. Discharge undermining represents a tissue space that remains in a pressure ulcer after discharge of liquefied necrotic tissue that is not preventable by nursing care. External force undermining has a profound bearing on external forces applied and can be prevented because it arises from a complex consisting of soft tissue movement toward a bony prominence and pressure. The healing time in external force undermining is significantly protracted compared to discharge undermining, and the external force should be eliminated to attain healing. The physician and nursing staff must recognize the 2 types of undermining that can develop in deep pressure ulcers, as well as underlying pathogenetic mechanisms. Care must be exercised to avoid pressure and shearing when changing the patient’s position and when raising the head side of the bed.References
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