The effects of pressure and shear on skin microcirculation in elderly stroke patients lying in supine or semi-recumbent positions.
The effects of external pressure and shear on the skin microcirculation over the sacral area, which is known as a high risk area for pressure sore formation, were studied in 30 elderly patients. The skin blood cell flux (SBF) was measured using the laser Doppler technique, with the patient first at rest in lateral position, then lying for 30 minutes in supine or semi-recumbent 45[degrees] position, and finally in lateral position.
Elderly high-risk patients (G2), most of them more than two years post-stroke, had a lower body mass index and a reduced sacral skin-fold compared with non-risk patients (G1). The SBF in G2 decreased 28% in supine and 14% in 45[degrees] position, whereas the SBF in G1 increased 35% in supine and 13% in 45[degrees] position. Spontaneous movements up to seven times per 30 minutes were registered, even during sleep, and were evident by direct observation of the recorded charts as a temporary SBF increase.
The risk for skin ischaemic damage over the sacral area of elderly risk patients was evident in both positions, especially with the patients lying in supine position. When increasing the upper body slope in G2 from horizontal to 45[degrees], an inability to recover a satisfactory blood supply after the ischaemic insult was found. Discomfort from compressive and shear forces initiates changes in posture, even in elderly patients prone to tissue breakdown. Occasional relief of pressure was in most patients followed by temporary increase in skin blood flow with concomitant temperature increase. This most probably protected them from developing skin lesions.
One of the prime mechanical factors for tissue breakdown of the skin, leading to pressure sore formation, is beyond question the external pressure over a bony prominence. In the clinical situation this pressure is exerted by the patient's own body weight against a hard layer. Clark and Rowland  measured the contact pressure between the sacrum and two different special mattresses and found that the mean pressures were higher for elderly subjects than for healthy volunteers. Reichel  pointed to shear effects as another prime factor for sacral pressure sores, and claimed that tilting the bed of paraplegic patients by only a few degrees was enough to cause arterial occlusion leading to tissue breakdown. Dinsdale  found in an animal study that when pressure was combined with shear, a lower pressure was sufficient to cause ulceration than when pressure alone was applied.
Important structural changes observed in elderly skin are reduction of the dermo-epidermal interface area, an increased vessel wall stiffness due to thickening of the basement membrane in the capillaries, and a loss of skin vascularity. Reduced tissue thickness and elasticity are morphological changes that predispose elderly patients to pressure and shear-type injuries , especially for sacral sores [5, 6]. The sacrum is a poorly perfused area in elderly patients, and a much lower external skin pressure was sufficient to stop the skin blood flow in the sacral area of elderly patients than over the gluteus muscle, while no such difference could be seen in younger volunteers . A low arterial blood pressure in elderly hospitalized patients was significantly correlated with occurrence of pressure sores . Reduction of the skin blood flow into the nutrient capillaries in a risk area will have a negative influence on the rate of oxygen transferred from the capillaries to the tissue. Even when moderate skin ischaemia occurs, plasma leaks through the wall of the dilated capillaries, causing local oedema. This oedema makes the skin less elastic and compromises the skin nutrition and eventually the capacity for wound repair.
The aims of the present study were to examine the effect of external pressure and shear on the microcirculation of ageing skin over the sacral area in a common clinical situation, using the laser Doppler technique, and to evaluate the interaction of these forces with the patient either in a supine or a semi-recumbent position.
Thirty elderly patients without pressure sores participated in the study. The patients were first assessed according to the Norton score  as being |not at risk' (score > 14), at |low risk' (score 14-12), or at |high risk' [score < 12] for development of pressure sores. The score includes five main variables such as physical and mental condition, mobility, activity, and continence. According to their scores the patients were divided into two groups.
Group 1 (G1) comprised 20 patients |not at risk' or at |low risk'. Ten patients were staying in a geriatric ward and ten were visiting a day-care unit for rehabilitation, mostly after fractures. Four patients were recovering from stroke and three patients had Parkinson's disease. Five patients were ambulant on their own, but the rest were mostly sitting in wheelchairs. Nine patients were incontinent.
Group 2 (G2) comprised ten elderly patients |at high risk', permanently institutionalized in a geriatric ward. Nine patients were recovering from stroke and one patient had Parkinson's disease. The patients with stroke were more than 2 years post-onset (range 2-7 years). One patient could walk independently but the rest were bedridden or sitting in wheelchairs. All patients were incontinent.
In the last decade, laser Doppler fluximetry (LDF) has been shown to be a useful tool for noninvasive continuous evaluation of transcutaneous microvascular dynamics , especially in clinical situations. The laser light, led by an optical fibre angle-probe to the skin, is reflected by blood flow both from superficial and deeper microvascular skin layers (Perimed[R] Fluxmeter PF 2B, Stockholm, Sweden). A double-sided tape fixed the angle-probe holder to the skin. In order to ensure that the probe did not influence the skin pressure, it was embedded in a specially designed foam rubber pad covered with terry cloth. The measurements were made at a bandwidth of 4kHz, a gain setting of x 100 and a time constant of 3 s, and were performed over the sacrum in an area about 10-12cm below a line between the iliac crest.
A thermistor probe lying on the skin, under the pad, monitored the skin temperature during the whole experiment. The thermistor was connected to an electronic thermometer with an accuracy of 0.1% (Anritsu Meter Co. Ltd, Tokyo, Japan).
The skin-fold thickness over the sacral area was measured after the SBF measurements with a Harpenden skin-fold calliper (British Indicators Ltd, Herts, England) to the nearest 0.2 mm. The calliper is designed to exert a constant pressure of 0.098 N/[mm.sup.2] [plus or minus] 10% at all openings of the 90 [mm.sup.2] anvils. The measurements were made twice over the sacrum, in an area about 10-1 2 cm below a line between the iliac crest and the mean value was calculated.
The arterial blood pressure of the right brachial artery was measured manually by the auscultatory method after 10min at rest. Duplicate measurements were made, and the mean value was calculated.
Body weight and height were measured by the hospital staff. The patients were weighed in light clothing without shoes. The body mass index (BMI), (also called Quetelet's index), was calculated as weight (kg)/square of height ([m.sup.2]). A BMI within the range 20-25 for men and 19-24 for women is considered as normal.
Measuring procedure. The investigation took place in a quiet room at a mean temperature of 22.9[degrees]C (range 21.4-25.4[degrees]C), and lasted for about 45 min which included equilibration time. No conversation was allowed during the investigation.
In the first part of the investigation the patient was lying in lateral position and the probes and the covering pad were placed on the skin over the sacral area. The temperature and SBF were then measured during resting conditions for 3 min. Five to seven SBF readings were taken, and the mean value was calculated (RF).
During the second part of the investigation the patient was lying either in supine position (defined as 0[degrees]) or in a semi-recumbent position with the trunk inclined (defined as 45[degrees]). The patient was lying on a standardized articulated board covered with a 25 mm foam rubber mattress. This stage lasted for 30 min, and temperature and SBF values were recorded every minute. The 0[degrees] and 45[degrees] tests were carried out on different days.
Finally, as the third part of the investigation, the patient turned to the lateral position again. At that time the LDF signal increased and a reactive hyperaemia (RH) response occurred in most patients. Rhythmic variations in the skin microvascular flow , known as flow motion activity (flow changes due to vasomotion), could be registered and the frequency component with the dominant amplitude was evaluated.
When spontaneous movements made by the patients occurred, they were marked on the recorder chart during the whole investigation.
Group SBF data are presented as mean value, standard deviation (SD), and standard error of the mean (SE). Normality tests were performed, which did not show any significant deviations from normal distributions. The group data were then compared using Student's t test. Five to seven different SBF values were measured during resting conditions and a mean value was then calculated. For each patient the SBF values during the second part of the investigation were normalized with respect to the mean SBF value during resting conditions according to the formula:
SBFn(%) = measured SBF value (AU)/mean SBF value at rest (AU) x 100
Changes in the normalized skin blood cell flux ([delta][SBF.sub.n]) and changes in the skin temperature ([delta]T) during the second and third part of the investigation were calculated by subtracting the mean value during resting conditions from the measured values.
This study was approved by the ethics committee, and all subjects or their families gave their prior informed consent.
Mean group data ([plus or minus] SD) are presented in the Table.
All patients in G2 were classified as being at high risk for developing pressure sores with a significantly lower score (p < 0.001) than in G1. The patients in G2 showed a lower BMI (p < 0.01) and tissue thickness over the sacrum area (p < 0.05) compared with G1. No significant differences in arterial blood pressures were found between the two groups.
There was no significant difference in SBF between the two groups during resting conditions or in day-to-day variations (G1: 16.5 AU; G2: 15.4 AU, NS).
For G1 in 0[degrees] position (Figure 1) the SBF successively increased, with a 16% rise after 11 min, and reached a maximum 35% above its initial value at the end of part two of the investigation, just before the patient was turned laterally again. For G1 in 45[degrees] position the SBF showed a fairly stable pattern during the first 10 min, then it successively increased by 13% at the end of stage two.
In contrast, for G2 in 0[degrees] position the SBF decreased rapidly to a minimum 28% below its initial value within 5 min, and in most patients did not reach its initial value before the end of stage two. Even in the 45[degrees] position the SBF for G2 decreased and reached a minimum 14% below its initial value within 10 min, whereas the SBF at the end of stage two reached its initial value in most patients.
After 30 min, when the patient was turned laterally, a transient overshoot of blood flow due to a reactive hyperaemia (RH) response followed in most patients.
Flow motion was evaluated during the first and the third stage of the investigation. There was no significant difference in flow-motion frequency between the two groups during resting conditions in the first stage of the investigation. Therefore, a comparison between the two positions was made with a pooled data set. During the RH response a strong flow motion started with a frequency within the range of 2-9 cycles/min (cpm). The flow-motion frequency during RH was significantly higher after the 45" position (6.8 [plus or minus] 2.6 cpm, p < 0.001) than during resting conditions (RF: 4.4 [plus or minus] 1.6 cpm), though the increase was within the normal range . No significant difference between flow-motion frequency during RF and RH after the 0[degrees] position was found. No further analysis of the SBF strength during RH could be made owing to spontaneous movements.
The patients made a number of spontaneous movements during the second stage of the investigation in both positions, up to seven times (Table) even during sleep, except for three of the four parkinsonian patients. No significant difference in the number of movements was found between the two groups in either position, though there was a tendency to more movements towards the end of the 30-min period. In most cases, these movements produced a transient increase in SBF, which was directly visible on the recorder chart (Figure 2).
[TABULAR DATA OMITTED]
In three patients with Parkinson's disease no spontaneous movements were registered at all. In these patients the LD signal during the second stage of the investigation fell to a level just above the zero value of the instrument, indicating a period of arterial occlusion.
The skin temperature was measured at the start (G1: 33.3[degrees]C; G2: 34.8[degrees]C) and during the whole investigation. The skin temperature increased in both groups and positions during the second stage of the investigation compared with its initial value (Figure 3). The increase was more pronounced in G1 (at 0[degrees]: 1.3 [plus or minus] 1.2[degrees]C, p < 0.001 and at 45[degrees]: 0.8 [plus or minus] 0.9[degrees]C, p < 0.001) in both positions than in G2 (at 0[degrees]: 0.6 [plus or minus] 0.7[degrees]C, p < 0.01 and at 45[degrees]: 1.5 [plus or minus] 0.6[degree]C, p < 0.01). The temperature was registered during the RH response and a temporary increase in 0[degrees] position was found, followed by a successive decrease in both groups concomitant with the SBF decrease.
Different hypotheses exist as to whether direct pressure or shearing forces or a combination of these forces act as the prime factor for pressure sore formation. Unfortunately, shear stress is not as easily observable as compressive stress, because shear forces mainly affect the vasculature in deeper tissue layers . The present study was carried out to evaluate the effects of pressure and shear stresses on the vascular supply to the sacral area, known as the main risk site for pressure sores. The investigation was designed so as to mirror a clinical situation, where elderly patients are either lying in bed or half-sitting during different occupations or exercises.
Differences in the SBF were found between the two groups and positions. In G1 a successive SBF increase was found in both positions though more prominent when increasing the slope of the body to 45[degrees]. In G2, on the contrary, the SBF decreased rapidly in both positions and hardly reached its initial value before the patient was turned laterally. It is known that in a semi-recumbent position the raised intramural pressure normally induces local reactive vasoconstriction of blood vessels. This local regulation tends to restore the blood volume which falls during recumbency . The at risk group which mainly comprised stroke patients showed an inability to recover a satisfactory blood supply compared with G1 when increasing their slope to 45[degrees]. This failure in G2 might be ascribed to vulnerability after their ischaemic insult.
The fast SBF decrease over the sacrum in G2, especially in the 0[degrees] position, contributed to obliteration of the skin microcirculation in most patients, causing a long-standing hypoxaemia. Reduced tissue oxygen pressure induces relaxation of terminal arterioles and precapillary sphincters, causing them to open when the oxygen concentration falls to low levels. At the relief of the external pressure, oxygen and nutrient-rich blood flushes into the skin capillaries. This reperfusion is an indication of recovery to meet the demands for repair. In most patients relief of the decompression of the vascular bed due to spontaneous movements was followed by a transient SBF increase which further contributed to a successively increased SBF (Figure 2).
It was previously found that the SBF in the sacral area during resting conditions and the reactivity of the skin microcirculation after a period of circulatory arrest was significantly impaired in elderly hospitalized patients compared with healthy subjects . This might identify patients at risk for developing pressure sores.
Rhythmic oscillations identified as flow motion (due to vasomotion) in the microvasculature were registered with a frequency of 2-9 cycles/min (cpm), both during the first and third stages of the investigation. Vasomotion is defined as spontaneous rhythmic changes in the diameter of the small vessels, produced by contraction and relaxation of the muscular components of their walls. Its activity is centrally mediated through hormones and the nervous system, and locally controlled by myogenic mechanisms. In terminal arterioles, vasomotion is postulated to be due to a local vascular pacemaker-like mechanism that can be influenced by the perfusion pressure . Vasomotion is important in distributing the SBF along the vascular tree and supplies oxygen and nutrients to ischaemic areas, washes away waste products, and serves as a positive influence in maintaining an effective venous outflow as well. Frequency values from the human nailfold capillaries have been reported to be in the range 4-10 cpm , and capillary flow velocity variations in animal preparations were reported to be synchronous with the activity of arterioles, whose frequency had the range of 5.4-9.5 cpm . A decreased frequency of vasomotion in active vessels was shown during the ageing of animal preparations , which may contribute to the low frequency seen in some recordings of elderly patients. The main part of the laser Doppler signal in the present study was generated from both superficial and deeper regions of the sacral skin. The recordings might thus mirror the effects on skin microcirculation from both pressure and shear.
Bader et al.  studied a patient lying on a surface inclined at 30[degreess] which would produce both shear and compressive force necessary to collapse the capillaries of the sacral area. They also evaluated the skin microvasculature of the forearm of healthy subjects using capillary miscroscopy, and found a progressive vascular collapse of both vertical and horizontal vessels with increasing force. Bennett et al.  found that the combination of pressure and shear affected the blood flow of the thenar eminence in such a way that the pressure needed to obtain a certain effect could be nearly halved when accompanied by sufficient shear. They also claimed that a sufficiently occlusive shear condition only develops under large compressive forces.
However, most previous studies on pressure and shear forces were made on healthy young subjects, in animal studies, or in a non-risk area, which do not reflect the @ common clinical situation with elderly disabled patients in bed.
Discomfort from compression of the skin readily initiates changes in posture. In most patients spontaneous movements occurred during the second stage of the investigation (Figure 2). This was surprising as there was no significant difference in the number of movements between non-risk and high-risk patients, except for three out of four with Parkinson's disease. These patients made no displacements whatsoever. Weller et al.  found a decrease in rotations at night among patients with Parkinson's disease compared with their healthy spouses. In clinical practice a common recommendation is that bedridden patients should be turned every 2 h, but according to our and their findings more individual recommendations should be considered for patients with certain diagnoses, such as Parkinson's disease or Parkinsonian-like states.
In the present study, movements were registered during day-time, with a mean value of 2-4 per 30 min. This corresponds to approximately 28-56 movements during a 7-h period. Exton-Smith and Sherwin  found that elderly patients who made spontaneous movements more than 54 times during a night period of 7 h were unlikely to develop pressure sores. Movement occurring during sleep is of particular importance, since sleep is metabolically the time for healing and repair. It was previously found that movements made by elderly patients were small and that high-risk patients made fewer movements than those who scored low risk [19, 20]. Movement of the body is simple to observe but it is difficult to determine which movements are relevant. Our study confirms that even elderly patients, confined to bed most of the time, were able to make small displacements affecting the SBF (Figure 2), which was visible on the recordings. These small movements restored oxygen and nutrient to pressure areas and might protect them from developing vascular damage.
An increase in temperature was observed in both groups and positions during the second stage of our study followed by a rapid temperature rise in some patients when they were turned laterally most clearly seen in the 0[degrees] position (Figure 3). Mahanty and Roemer  found that the temperature rise associated with reactive hyperaemia increases with increase in pressure magnitude and duration. When a patient is lying in bed on a plastic mattress cover, increased temperature and humidity, most probably due to lack of evaporation and to incontinence, will further affect the SBF and raise the oxygen need of the tissue.
Beside a low Norton score, the high-risk patients had a significantly lower BMI and sacral skin-fold than did the non-risk group. An even lower sacral skin-fold was found in elderly patients with pressure sores over the sacrum . Subcutaneous fat is decreased in malnourished patients, and their skin is not cushioned to resist pressure. A reduced tissue thickness over the sacrum will further increase the effects of pressure and shear on the skin microcirculation. Schubert and Fagrell  evaluated the local pressure effects on the skin microcirculation of healthy subjects and found that a local pressure of 110 mmHg (14.6 kPa) over the sacrum reduced the SBF more than over the gluteus muscle. Seiler and Stahelin  recommended that elderly patients should be moved to a 30' lateral position in order to avoid external pressure on the sacrum and the heels. In this position the pressure effects may be distributed to the gluteus muscle.
In conclusion, this study has confirmed the potential danger from compressive and shear forces to skin perfusion. The risk for skin ischaemic damage over the sacral area of elderly high risk patients was evident in both positions, but was most prominent in the supine position. Discomfort from these forces initiates changes in posture, even in elderly patients prone to tissue breakdown. Occasional pressure release was in most patients followed by a small transient skin blood flow increase, which most probably protected them from developing skin lesions. Our findings favour the hypothesis of compressive force as the main external risk factor for developing tissue damage in the sacral area.
This study was supported by grants from the Karolinska Institutet, the Foundations for Aging Research, Gun and Bertil Stohne and |Gamla tjanarinnor'.
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|Author:||Schubert, V.; Heraud, J.|
|Publication:||Age and Ageing|
|Date:||Sep 1, 1994|
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