Catherine Anne Sharp
Last updated: Oct 2005
Keywords: Pressure ulcers; ischaemia reperfusion injury; staging; grading; repositioning; evidence-based practice.
Evaluations of pressure damage are usually based on the traditional top-to-bottom model of classifying or staging pressure ulcers, beginning with damage to the surface of the skin and working down to the bone in stages according to the visible depth of tissue damage. The authors question the veracity of this model and propose a new approach called 'the middle model'.
Recognising that time/pressure relationships for the development of pressure ulcers can differ widely between individuals means that the strict implementation of local guidelines on the frequency of repositioning could put at risk those patients who are most vulnerable to developing a pressure ulcer.
The authors propose that less emphasis should be placed on assessment of the skin for the risk of pressure ulcer development and that instead the focus should be on assessment of the single most evidence-based predictor - immobility.
This paper aims to promote discussion on the physiology of pressure ulcer development and the impact this may have on clinical intervention and the allocation of resources. It argues against the use of both the Australian Wound Management Association's  and the New South Wales Department of Health's  method of staging pressure ulcers, which is similar to the grading system established by the European Pressure Ulcer Advisory Panel (EPUAP) , as a tool for assessing the risk of pressure ulcer development and the only tool for evaluating the severity of pressure damage.
It proposes a new model ,'the middle model', whereby tissue damage may start anywhere between, and including, the skin surface and bone interface, concurrently or haphazardly, to produce a pressure ulcer.
About 60,000 people in Australia have at least one pressure ulcer at any given time  as a result of unrelieved pressure, friction or shear forces  . Yet it is estimated that over 80% of these could be prevented if appropriate interventions were initiated as soon as patients became immobile .
The annual cost of treating pressure ulcers in Australia is thought to be more than $350m  (about £145m), but the cost of treating a single Stage IV pressure ulcer [Table 1] has been estimated at $61,230 (about £25,000), excluding the cost of the pre-existing admitting condition . In addition, legal action has the potential to vastly inflate associated costs.
It is widely accepted that pressure ulcers can develop as a result of prolonged periods of immobility          , during which unrelieved pressure compresses tissues that often overlie bony prominences        . This has the potential to cause full-thickness skin lesions that can destroy muscle and sometimes bone. In an attempt to prevent this, nurses usually reposition patients every two hours, when they also assess the skin for evidence of pressure damage. Any skin assessment should take into account the presence of erythema, or non-specific redness of the skin. On intact skin, persistent erythema, with or without changes in skin temperature, indicates a Stage 1 pressure ulcer according to the New South Wales Health Department's classification system [Table 1].
If erythema persists it is generally recommended that patients should be repositioned more frequently. This evaluation and intervention is based on the traditional top-to-bottom physiological model of pressure ulcer development , which assumes that damage begins at the surface of the skin, working down to the bone in stages according to the visible depth of tissue damage.
The more recent bottom-to-top model    suggests that damage begins at the bone and works up through the muscle toward the skin, with visual assessment of the skin giving no indication of the extent of underlying tissue damage.
However, relieving pressure on any part of the body may cause reactive hyperaemia, a protective response normally observed after arterial occlusion  . This may be noted during repositioning and appears as erythema: redness or flushing of the skin that was under pressure caused by the reflux of arterial blood. Once the erythema has disappeared, it is wrongly assumed that the potential for serious damage to the blood vessels in both immobile and healthy mobile subjects no longer exists .
Persistent erythema that does not whiten when light pressure is applied to the skin is known as non-blanchable erythema and may be accompanied by changes in skin temperature and consistency, and/or itching. In such cases practitioners who use staging or grading systems to indicate the depth of tissue damage    would usually identify a Stage I (or Grade 1) pressure ulcer.
Unlike the discolouration produced by reactive hyperaemia, non-blanchable erythema is significantly associated with the development of pressure ulcers  so it is important to clarify the difference between these two terms, which are often used interchangeably  . For the purpose of this paper we classify reactive hyperaemia as a normal response following arterial occlusion   and non-blanchable erythema as an abnormal response, presenting as the 'persistent redness' that characterises a Stage I pressure ulcer [Table 1]  .
In clinical practice it may be difficult to distinguish between the discolouration of non-blanchable erythema and that caused by reactive hyperaemia, which can make a reliable assessment of the skin difficult . The ambiguity associated with these terms is the result of two common misconceptions. First, reactive hyperaemia and non-blanchable erythema are often mistaken   . Second, non-blanchable erythema is often seen as an indication of risk rather than of the presence of pressure damage   . This was borne out by a survey of nurses in Sydney, Australia, which found that more than a quarter of them considered that, because the skin remained intact, classification of skin damage as Stage I was a risk factor for the development of pressure ulcers .
Stage I changes in the skin should not be relied upon to indicate the beginning of the pressure ulcer development process as irreversible damage to the deep tissue can occur before Stage I. For this reason the authors propose the inclusion of a 'pre-Stage 1' based on physiological changes that indicate the non-visible commencement of pressure ulcer development.
A search of peer-reviewed publications began with the 1958 seminal work by Michael Kosiak , which reported the development of pressure ulcers in humans as a result of ischaemia. The search included the use of the Medline, Cochrane and Cinahl databases. The paucity of publications listed on Index Medicus necessitated an additional springboard search, from references in papers listed on Index Medicus to internet-based special interest healthcare groups that listed conference abstracts.
The staging method for pressure ulcer development currently in use in Australia includes two main physiological models. The traditional top-to-bottom model  for staging pressure ulcers is recommended in Australia but there is growing acceptance that the invisible bottom-to-top model    does cause or contribute to pressure ulcer development. Numerous factors are thought to play a part in the development of pressure ulcers but this paper will focus on the three main ones: pressure, friction and shear. These are common to both the Australian Wound Management Association's framework for pressure ulcer prevention  and the New South Wales Health Department's guidelines for all healthcare facilities .
Table 1 shows the traditional system of staging pressure ulcers in Australia.
|l||Observable pressure-related alteration(s) of intact skin
whose indicators as compared to the adjacent or opposite area on
the body may include changes in one or more of the following:
||The ulcer appears as a defined area of persistent redness in lightly pigmented skin; in darker skin tones it may appear with persistent red, blue and/or purple hues.|
Partial-thickness skin loss involving epidermis and/or dermis.
|The pressure ulcer is superficial and presents clinically as an abrasion, blister or shallow crater. (Note: such superficial presentations may also represent a non-pressure related injury due to friction and excessive moisture as a result of, for example, incontinence, wound drainage, perspiration.)|
|lll||Full-thickness skin loss involving damage or necrosis to subcutaneous tissue and extending down to, but not through, the underlying fascia.||The ulcer presents clinically as a deep crater with or without undermining of the adjacent tissue.|
|lV||Full-thickness skin loss with extensive destruction, tissue necrosis or damage to muscle, bone, or supporting structures (for example tendon or joint capsule).||Undermining and sinus tracts may also be associated with Stage IV pressure ulcers.|
Although staging is recommended in all Australian healthcare facilities  , anecdotal evidence suggests that this system is not well understood or used. Ischaemia reperfusion injury, the focus of the middle model proposed in this paper, may be an additional factor in the development of pressure ulcers. Based on non-visible physiological changes that take place before Stage 1, its acceptance as an important part of the pressure ulcer development process would necessitate a review of the current classification system.
When pressure is transmitted from any type of surface, such as a mattress or chair, damage is traditionally thought to start at the skin, progressing down to the blood vessels, then to the subcutaneous fat, muscle and eventually the bone. This is known as the top-to-bottom model of pressure ulcer development . The Australian staging system is based on this model. The bottom-to-top model hypothesises that pressure ulcer development begins in the deeper tissues near the bone, occurring when increased pressure damages skeletal muscle, subcutaneous fat and blood vessels, before becoming evident at the skin surface   . This explains how the extensive tissue damage described in Stage IV of the top-to-bottom model may be concealed by intact skin, which would traditionally be categorised as a Stage I ulcer.
The main risk factors associated with the development of pressure ulcers are traditionally thought to be:
In both the models described above, the development of a pressure ulcer is thought to result from a complex relationship between these three risk factors and other causal factors, including ischaemia due to unrelieved pressure        , how often pressure is applied      and the length of time tissue is subjected to pressure           , the shearing of tissues       and the reperfusion of ischaemic tissue     leading to tissue necrosis   . Each of the three main risk factors will be considered alone before their relationship with other factors is discussed. However, the literature search carried out for the purposes of this paper revealed a lack of evidence on the role of friction in the development of pressure ulcers.
When external pressure exceeds internal capillary pressure over the bony prominences of the pelvis, such as the sacrum           , buttocks    , coccyx   , ischial tuberosities    and heels      , patients who cannot change position are at risk of developing a pressure ulcer          . Anaesthetised patients are one example of immobile people who are at risk because they are unable to sense the discomfort of pressure and initiate movement    . Anaesthetised patients on operating theatre tables, as well as patients on emergency department trolleys and hospital mattresses, are subjected to interface pressures much higher than the 28-38mmHg still considered by some to be a safe level of pressure in healthy subjects . Extremely high pressures have been recorded between such patients' skin and support surfaces, with 56-60mmHg over the sacrum of a patient on an emergency department trolley and 75-80mmHg over the sacrum of an anaesthetised patient on an operating theatre table .
Occipital tissue interface pressures higher than 32mmHg have been recorded in patients undergoing coronary artery by-pass graft surgery and resulted in tissue ischaemia in areas of skin over bone . Skin over bone has been reported to have a significantly (p<0.001) stiffer load deformation relationship than skin over muscle, but interestingly the subcutaneous pressure required to reduce the all-important transcutaneous partial pressure of oxygen (TcPO2) was not significantly different (p>0.05) for skin over muscle (36+/-11mmHg; mean+/-standard deviation) than for skin over bone (28+/-10mmHg) .
This supports the contention that patients who are at risk of developing a pressure ulcer need to be protected from unrelenting pressure to all parts of their bodies, including soft tissue as well as bony prominences because the skeleton lies on top of soft tissue in any body part under pressure. The level of pressure required to cause damage varies from person to person, according to factors such as location and disease process. For example, what is considered a tolerable level of pressure in some people may be too high for patients with peripheral vascular disease (PVD) who may develop an ulcer in a very short period of time if they are immobile  . Conversely, mobile patients with PVD may trigger many more lower-limb movements (73+/-50 an hour) than healthy subjects (11+/-12 an hour), possibly due to the body's physiological attempt to increase blood flow to the lower limbs . If movement was not possible in these patients the result might be the rapid development of a pressure ulcer.
This time/pressure relationship was initially reported in dogs, with ischaemic ulcers developing after pressures of 60mmHg were applied for one hour . Subsequent studies of the time/pressure relationship in healthy volunteers concluded that variations in hyperaemic responses were due to intrinsic physiological differences . This may explain why a group of 16 patients aged over 60 with atherosclerotic disease responded differently to pressure applied for one hour. Four showed no change in blood flow, four had increased skin blood flow to ≥150% of baseline flow and eight had decreased skin blood flow to ≥50% of baseline flow, with three of these having a final blood flow of zero . It is, therefore, conceivable that patients with morbid conditions may respond differently, and faster, with regard to the time/pressure relationship in pressure ulcer development.
Time from unrelieved pressure to evidence of pressure ulcer development ranges from a matter of hours  to days       or even two    to three weeks   . This relationship varied widely in a group of 44 patients who developed a total of 70 pressure ulcers in the first two days after surgery, with 12 Stage I ulcers observed immediately after surgery . These deteriorated to a higher stage in nine patients who were followed up for only six days after surgery . Yet 25 ulcers deteriorated to a higher stage in 13% of those initially identified with a stage 1 pressure ulcer who were followed for up to two weeks . It would appear that, at the very least, follow-up of three weeks  is necessary to determine the true incidence of pressure ulcers, which may take more than six days to manifest. This study also suggests that examining the skin at the time of repositioning may underestimate the time/pressure effect.
Finally, discrepancies in the outcomes of individuals subjected to similar conditions may be due mainly to the confounders presented by clinical support surfaces, which have a different effect on people of different heights and weights. For example, a small, light person may comfortably sink into a soft surface without high pressure being created over bony prominences, whereas the same surface may result in extremely high pressures on soft tissues over the bony prominences of a large, heavy person .
Friction, which is the resistance created when one surface is rubbed against another, is generally acknowledged as one of the main mechanical causes of pressure ulcers but an examination of the literature did not reveal any evidence that friction per se is a causal factor. However, friction on wet skin can result in persistent redness, which is often incorrectly classified as a Stage I pressure ulcer, regardless of mobility. The term friction is often confused with the term shearing, which places both skin and deep tissue at risk of pressure ulcer development.
Skin moisture in itself does not have a direct causal link to the development of a pressure ulcer but moisture may be an important factor when it acts as an effect modifier by restricting normal blood flow, from 0.01±0.007pu in dry skin to 0.04±0.009pu in skin wet with synthetic urine .
Further research is needed to establish the role of friction in the development of pressure ulcers and the precise nature of its interaction with other exacerbating factors, such as moisture.
Shearing is potentially the most serious of the three main risk factors because of the speed with which tissue damage occurs. The term describes a mechanical force on the skin's surface extending into the bony skeleton that acts in parallel rather than perpendicular to an area of tissue , for example when the tissue over bony prominences is dragged against a surface when an anaesthetised patient is moved across an operating table . In older patients the effects of shearing may be exacerbated by loose, fragile tissue, where the elasticity of the thinning epidermis has diminished and dermal blood vessels have been lost , with the result that tissue is sheared or dragged away from its attachment to the bone and local blood vessels are avulsed . In day-to-day patient care there is no reliable method of estimating the potential for shearing or the resultant damage .
Ischaemia occurs when blood flow to the tissues is inadequate, resulting in cell death and tissue necrosis. When a patient is repositioned, it is expected that the skin previously under pressure will reperfuse   . But in the same way as the time it takes for an ulcer to develop may vary, capillary closing pressures that may result in tissue ischaemia also vary          .
In a study to test the effects of intermittent pressure, the skin of 18 pigs was subjected to four-hourly cycles of 210 minutes of pressure followed by 30 minutes of pressure relief over 48 hours. Blood flow was significantly decreased (p<0.01) and resulted in pressure ulcers in all of the pigs at 48 and 72 hours. One pig was followed up for three weeks. Interestingly, the lesions began as areas of non-blanchable erythema and progressed according to the top-to-bottom model, with eventual sloughing of necrotic skin and muscle, leading the authors to conclude that the ulcers were caused by repeated interruption of the capillary closing pressure .
Normally, reperfusion after stasis of blood flow caused by external pressure will lead to reactive hyperaemia and the restoration of normal vascular tone can be measured by skin temperature. Excellent reperfusion was demonstrated in healthy volunteers whose post-pressure temperature increased by an average of 3.4°F (p=0.01) compared with their pre-pressure temperature . After two hours of unrelieved pressure, the same study found good reperfusion in patients in intensive care who could move independently when their post-pressure skin temperature increased significantly (p=0.03) by 0.83°F. However, the post-pressure skin temperature of patients who lacked independent movement did not increase . So little or no change between pre- and post-pressure skin temperatures may indicate inadequate or no reperfusion of tissue.
Prompt reperfusion of ischaemic tissue is crucial to restoring normal function, but if there is existing pressure damage reperfusion can precipitate a progressive destruction of the cells, leading to paradoxical tissue dysfunction and necrosis    , a phenomenon known as ischaemia reperfusion injury   . If there is existing pressure damage, reperfusion can result in irreversible cellular damage with tissue dysfunction and necrosis   .
Ischaemia can cause irreversible damage if it activates the inflammatory response      and has been demonstrated in pigs , whose skin is similar to that of humans. In this complex response damage is caused by white blood cells, lipid-derived mediators and free radicals   . There is evidence of a relationship between ischaemia and reactive hyperaemia, as a result of cycles of pressure and pressure relief, resulting in ischaemia reperfusion injury and causing pressure ulcers in animals     . However, an extensive online search using the Cinahl, Medline and Cochrane databases did not identify any papers associating ischaemia reperfusion injury with pressure ulcers in humans.
Ischaemia reperfusion injury has, however, been reported in many human organs, such as the heart and brain , and the liver . When blood flow is not fully restored after the release of vascular occlusion this may manifest as focal areas of stasis , with the potential for tissue injury or continued organ dysfunction, such as the failure of a transplanted graft, in the post-reperfusion period . It is, therefore, possible that Stage IV pressure ulcers [Table 1] may result not only from pressure and shearing but also from ischaemia reperfusion injury to skin and skeletal muscle.
Both the top-to-bottom and bottom-to-top models present coherent and plausible explanations for pressure ulcer development but fail to consider the crucial role of ischaemia reperfusion injury in compromising blood flow, which can lead to tissue hypoxia, interstitial haemorrhage and cellular death . Assessing for reactive hyperaemia using a visual assessment for redness and palpating the skin to monitor changes in temperature compared with adjacent tissues is based on the top-to-bottom model, but neither of these models may be wholly predictive of pressure ulcer development.
With the top-to-bottom model   becoming less convincing as the sole construct of pressure ulcer development and no clear alternative, it is understandable why the visible damage defined in Stage I is commonly used to assess the depth of tissue damage and to identify patients at risk of developing a pressure ulcer. However, this model does not allow for the consideration of other constructs of pressure ulcer development, such as the bottom-to-top model or ischaemia reperfusion injury.
If other constructs for pressure ulcer development are accepted then Stage I or Grade 1 should be redefined as 'pre-ulcerative changes' in accordance with the visual ulcerative state described by Eltorai . For construct validity, Stage I or Grade 1 should be renamed 'Pre-ulcerative changes', with Stage II or Grade 2 becoming Stage 1 and Grade 1, and so on.
As credible as the bottom-to-top model is   , including as it does important constructs of unrelieved pressure, shearing forces and resultant ulcer development, it does not specifically include ischaemia reperfusion injury. Therefore, we propose a third model, the middle model, whereby tissue damage may start anywhere between, and including, the skin surface and bone interface, concurrently or haphazardly, to produce a pressure ulcer.
In examining the evidence for the recommended current conceptual framework for staging   [Table 1], it is important to appreciate the risk of accepting the top-to-bottom model   as the only order of progression in pressure ulcer development. This traditional view discounts the potential for shearing forces to avulse and occlude blood vessels, possibly preventing the optimal reperfusion of tissues under pressure, all of which occurs unseen in the bottom-to-top model   .
While the assessment of skin appearance is a valuable indicator of tissue trauma, the findings of several studies challenge the traditional view that pressure ulcer development necessitates progression through each stage   . Schoonhoven et al found that blanchable erythema, or Stage I, did not precede a total of 23 Stage II pressure ulcers . And although the association between the persistent redness of intact skin and pressure ulcer development is not being challenged, a lack of skin redness does not necessarily indicate an absence of risk or rule out the possibility of a deep ulcer   developing from bottom to top. A visual assessment of skin integrity should occur each time the patient is repositioned   , but this is currently used to determine the existence and extent of pressure damage and is erroneously considered an important preventive management strategy    . The danger is that preventive strategies may be implemented too late for patients without skin redness . The evidence of ischaemia reperfusion injury in animals     and various organs in the human body    is indisputable, supporting the validity of the proposed middle model as a construct for the formation of pressure ulcers in the largest organ of the body, the skin.
Many practices that are not based on evidence are perpetuated in the literature on pressure ulcers. The misuse of terms such as 'friction and shearing', 'reactive hyperaemia' and 'non-blanchable erythema' causes confusion that may have contributed to the acceptance of less than optimal practice.
After examining the literature, the authors conclude that the recommended practice of assessing the skin for evidence of pressure damage when repositioning patients is not evidence-based.
Assessing the skin for evidence of pressure damage when repositioning patients is good practice, but there is no evidence that using visual assessment to stage or grade pressure ulcers according to the recommended criteria is a reliable system of classification.
Given the problem of individual time/pressure relationships for the development of pressure ulcers, if the middle model is correct the frequency with which patients are repositioned should be determined solely on the basis of individual need and circumstances.
Seeking to protect patients from ischaemia reperfusion injury is not new and has been associated with myocardial infarction, cardiopulmonary bypass  and the preservation of organs for transplantation . Using alternating pressure surfaces to relieve pressure at five-minute intervals helps to prevent ischaemia reperfusion injury and has consistently been shown to minimise tissue damage  . However, just over half (54%) of the nurses surveyed in a large area health service in Sydney reported that there were insufficient support surfaces, such as alternating pressure air mattresses, to meet the needs of patients at risk of developing pressure ulcers. As a result, most of them (89%) continued to reposition patients every two hours .
It is more than 40 years since the publication of findings that 90% of older patients who made fewer than 10 movements on their own over a seven-hour period at night, resulting in a change of pressure once every 42 minutes, developed a pressure ulcer . The same study found that those who did not develop one made 54 movements in the same time period, moving every seven to eight minutes in one 420-minute period during the night. More recently, it has been suggested that patients need to be repositioned every few minutes . If repositioning every seven to eight minutes would prevent pressure ulcers, in immobile patients this would have to be done 180-205 times in each 24-hour period. This is an unattainable goal on any ward.
For some patients, the standard practice of two-hourly repositioning may need to be continued for weeks, months or even years, perpetuating the cycle of intermittent pressure on certain areas of the body and increasing the potential for ischaemia . Tissue damage occurs rapidly and has been noted after less than one hour of unrelieved pressure , but for hard-pressed healthcare practitioners the frequency of repositioning required to prevent most pressure ulcers is simply impractical.
Further research is needed to establish the link between ischaemia reperfusion injury and the development of pressure ulcers in humans and to create an evidence base for the repositioning of patients - every two hours is a practice that has yet to be evaluated.
Time/pressure factors and ischaemia reperfusion injury form a complex physiological relationship that may differ significantly from patient to patient. It is fair to assume that the development of pressure ulcers is a result of the same phenomenon, known as ischaemia reperfusion injury, that has been described in relation to other human organs     and in the development of pressure ulcers in animals . There is little published evidence to demonstrate that two-hourly repositioning, a mainstay of nursing practice, is an effective method of pressure sore prevention or that it does not contribute to ischaemia reperfusion injury.
The authors suggest that the development of a pressure ulcer is not simply a top-to-bottom process: it may occur from bottom to top, according to the middle model or, most likely, is a combination of all three. However, this raises practical problems as it is impossible for clinicians to know whether a Stage I pressure ulcer really is superficial or whether the appearance of the skin is the result of ischaemia reperfusion injury.
Although skin assessment can be a valuable indicator of tissue trauma, the findings of several studies challenge the traditional view that pressure ulcer development necessitates progression through each of the four stages described in Table 1. If pressure ulcers develop as a result of all three models, several current clinical practices are ad hoc rather than evidence-based, including repositioning regimens, diagnoses based on visual assessment for persistent redness of the skin and palpating for temperature changes.
The focus of any skin or pressure ulcer risk assessment should move from using a staging system, which on its own is an inadequate evaluation tool, to the most evidence-based predictor of pressure ulcer development - immobility. Frequent repositioning cannot guarantee the prevention of ischaemia reperfusion injury and may contribute to this phenomenon so the widespread introduction of alternating pressure air mattresses, which intermittently create areas of reduced pressure, needs to be evaluated.
Further research and the evaluation of evidence are urgently required to determine the process and progress of ischaemia reperfusion injury in relation to pressure ulcer development in humans. Given the paucity of evidence on the role of friction, which is generally considered one of the main causal factors in the development of pressure ulcers, specific research is also needed to clarify the nature and extent of its effect on the skin, alone and in combination with other contributing factors.
These issues need to be addressed and debated before firm recommendations for practice can be made. However, until adequate resources are provided for the widespread introduction of appropriate pressure-relieving devices, less effective measures such as two-hourly repositioning and skin assessment will remain the mainstay of pressure ulcer prevention.
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