| Title | Skin circulation in areas prone to pressue ulcerationand adjacent nonsusceptible areas as determined by the thermal recovery method |
| Publication Type | thesis |
| School or College | College of Nursing |
| Department | Nursing |
| Author | Hedegaard, Vern |
| Date | 1984-03 |
| Description | Pressure ulcers, also called decubitus ulcers and bed sores, are areas of hypoxemic necrosis resulting from compression of capillaries by externally applied pressure. They most commonly develop in areas of the body subjected to prolonged high pressure, such as the trochanters, sacrum and ischia. Very little is known about the local skin circulation in these areas. Reduction of the magnitude and duration of pressure applied to the body surface have been shown to be effective, scientifically based nursing interventions. Interventions based on increasing skin blood flow, although commonly used, have not shown to be effective or scientifically based. The purpose of this study was to compare the skin circulation of areas prone to pressure ulceration with the skin circulation of adjacent, less susceptible areas. The thermal recovery method was use to estimate the skin blood flow over the trochanter and sacrum, and compared to that over the abdomen and groin. No significant differences were found between the thermal recovery values of the trochanter and groin, or between those of the sacrum and abdomen. Although subject's thermal recovery values varied widely, no significant differences were observed based on site, age, sex, diastolic blood pressure, or height/weight ratio. The results of this study indicate a need for continued study of the skin circulation of areas prone to pressure ulceration. The conclusion of other studies utilizing skin temperature as an index of circulation require reexamination. The emphasis in nursing intervention should continue to be directed toward relieving pressure, rather than increasing skin circulation. |
| Type | Text |
| Publisher | University of Utah |
| Subject | Blood Supply |
| Subject MESH | Skin; Decubitus Ulcer |
| Dissertation Institution | University of Utah |
| Dissertation Name | MS |
| Language | eng |
| Relation is Version of | Digital reproduction of "Skin circulation in areas prone to pressue ulcerationand adjacent nonsusceptible areas as determined by the thermal recovery method." Spencer S. Eccles Health Sciences Library. Print version of "Skin circulation in areas prone to pressue ulcerationand adjacent nonsusceptible areas as determined by the thermal recovery method." available at J. Willard Marriott Library Special Collection. QP 6.5 1984 H43. |
| Rights Management | © Vern Hedegaard. |
| Format | application/pdf |
| Format Medium | application/pdf |
| Format Extent | 1,126,714 bytes |
| Identifier | undthes,4862 |
| Source | Original: University of Utah Spencer S. Eccles Health Sciences Library (no longer available). |
| Master File Extent | 1,126,736 bytes |
| ARK | ark:/87278/s6g44s42 |
| DOI | https://doi.org/doi:10.26053/0H-6YHR-AVG0 |
| Setname | ir_etd |
| ID | 191416 |
| OCR Text | Show SKIN CIRCULATION IN AREAS PRONE TO PRESSURE ULCERATION AND ADJACENT NONSUSCEPTIBLE AREAS AS DETE~1INED BY THE THERMAL RECOVERY NETHOD by Vern Hedegaard A thesis submitted to the faculty of The University of Utah in partial fulfillment of the requirements for the degree of Master of Science College of Nursing The University of Utah March 1984 © 1984 Vern Hedegaard All Rights Reserved THE UNIVERSITY OF UTAH GRADUATE SCHOOL SUPERVISORY COMMITTEE APPROVAL of a thesis submitted by Vern Hedegaard This thesis has been read by each member of the following supervisory committee and by majority vote has been found to be satisfactory. Chamnan: Sue E. Huether, R. N ., Ph. D. James S. Wood, M.D. THE UNIVERSITY OF UTAH GRADUATE SCHOOL FINAL READING APPROVAL To the Graduate Council of The University of Utah: 1 have read the thesis of Vern Hedegaard in its final form and have found that (1) its format. citations. and bibliographic style are consistent and acceptable; (2) its illustrative materials including figures. tables. and charts are in place; and (3) the final manuscript is satisfactory to the Supervisory Committee and is ready for submission to the Graduate School. ~ /~,)1tY Dale J Sue E. Huether, R.N., Ph.D. Member. Supervisory Committee Approved for the Major Department Linda K. Amos, Ed.D., F.A.A.N. Chairman D(an Approved for the Graduate Council ABSTRACT Pressure ulcers, also called decubitus ulcers and bed sores, are areas of hypoxemic necrosis resultinq from compression of capil by externally appl pressure. They most commonly develop in areas of the body subjected to prolonged high pressure, such as the trochanters, sacrum and ischia. Very little is known about the local skin circulation in these areas. Reduction of the magnitude and duration of pressure applied to the body surface have been shown to be effective, scientifically based nursing interventions. Interventions based on increasing skin blood flow, although commonly used, have not been shown to be effective or s entifically based. The purpose of this study was to compare the skin circulation of areas prone to pressure ulceration with the skin circulation of adjacent, less susceptible areas. The thermal recovery method was used to estimate the skin blood flow over the trochanter and sacrum, and compared to that over the abdomen and groin. No significant f rences were found between the thermal recovery values of the trochanter and groin, or between those of the sacrum and abdomen. Although subjects' thermal recovery values varied widely, no significant differences were observed based on site, age, sex, diastolic blood pressure, or height/weight ratio. The results of this study indicate a need for continued study of the skin circulation of areas prone to pressure ulceration. The conclusions of other studies utilizing skin temperature as an index of circulation require reexamination. The emphasis in nursing intervention should continue to be directed toward relieving pressure, rather than increasing skin circulation. v CONTENTS ABSTRACT. . . . LIST OF TABLES. ACKNOWLEDGMENTS . Chapter I . II. III. IV. INTRODUCTION AND LITERATURE REVIEW . Introduction .... Review of the Literature . CONCEPTUAL FRAMEv.70RK . Assumptions ...... . Conceptual Framework .. ... Research Questions . . . . . . Operational Definitions .. METHODOLOGY AND RESEARCH DESIGN .. Aim. . . . . . . . . . . . . . . . Population . Design . . . . . . Instruments. . . ...... . Data Collection Procedures . Data Recording . . . . . . . Overview of Data Collected . . DATA ANALYSIS. . Methods of Data Analysis Descriptive Statistics . . Paired t-Test ..... . Results-of Data Analysis . scussion . . . . . . . Implications for Nursing Practice .. iv . .viii x 1 1 5 29 29 29 32 32 34 34 34 35 35 37 38 41 43 43 43 44 46 66 81 v. SUW'lARY AND RECO:t-1MENDATIONS. 84 Summary. . . . . . . . . .. ... 84 Recommendations for Further Research . . . 86 Appendices A. INFORMED CONSENT FORM. . . B. THERMOMETER AND THERMISTOR SPECIFICATIONS . . . . . . . . C. DATA COLLECTION SHEETS . D. PROTOCOL . . . . E. MEAN TEMPERATURE VALUES. 89 91 93 97 . 101 REFERENCES ..................... 116 Vll LIST OF TABLES 1. Study Population Characte s tics. . 2. Ini al Skin Temperature (0 C) ... 3 . t-Statistics and E-Values: Initial Skin Temperatures ....... . 4. Decrease in Skin Temperature (0 C) Following Application of Cold . 5. 6 • t-Statistics and p-Values: Decrease in Skin Temperature.-..... Skin Temperatures at Experimental and Control Si tes (Phase I) . . . . . 7. Skin Temperatures at Experimental and 47 50 51 52 54 55 Control Sites (Phase II). . . . . . . . . . . . 56 8. Peripheral Blood Circulatory Index Trochanter and Groin. . . . . . . . 9. Peripheral Blood Circulatory Index Sacrum and ~~domen ......... . 10. Two Sample t-test (Unequal Variance) PBCI Male and Female .. 11. ANOVA of PBCI by Age .. 58 59 60 61 12. ANOVA of PBCI by Diastolic Blood Pressure . 62 13. 14. ANOVA of PBCI by Height/vJeight Ratio. Two Sample t-test (Unequal Variance) PBCI Right and Left Trochanter .... 63 64 15. Correlation Hatrix: PBCI Experimental Sites.. 65 16. Correlation Coefficients Initial Temperature Decrease versus PBCI. 67 17. Baseline Skin Temperatures (0 C) : (n=50) and Present Study (n=30) .. ix Howell • • • 72 ACKNOWLEDGMENTS The author extends sincere appreciation to the members of the Supervisory Committee, Mary Ann Johnson, R.N., M.S. and James S. Wood, M.D. for their continued support and encouragement. A special thank-you is extended to Sue E. Huether, R.N., Ph.D., Chairperson of the Supervisory Committee, without whose diligent efforts and technical contributions, this project would not have been possible. CHAPTER I INTRODUCTION AND LITERATURE REVIEW Introduction Pressure ulcers, also known as decubitus ulcers and bed sores, are areas of necrotic tissue caused by the application of prolonged, elevated pressure to the affected area. They are a common nursing problem, and estimates of their incidence in hospitalized patients range from 3.0% (Barbanel, Jordan & Nichol, 1977) to 8.8% (Peterson & Bittman, 1971). The inci-of pressure ulcers in geriatric facili is probably even higher. One estimate is that 20% of the patients in such a facility will develop a pressure ulcer sometime during their stay (Isiandinso, 1979). Pressure ulcers are not benign. Once the ulcer has developed, the care of the patient is time-consuming and costly. The average length of hospitalization required for the treatment of pressure ulcers in one spinal is unit was three months (McClemont, Shand & Ramsey, 1977). In 1979, the cost of treating a single pressure ulcer was estimated to be $14,000 2 (Nola & Vistnes, 1980), with infection, sepsis, and death as the most serious complications. In one series, 48% of all patients with septicemia due to pressure ulcers died (Galpin, Chow, Bayer & Guze, 1976). Pressure ulcers occur in areas of the body subject to anoxic necrosis. When pressure exceeding capillary intraluminal pressure applied to the surface of the body, the pressure transmitted to the capillaries, and capillary flow is interrupted. If the duration and magnitude of pressure application are sufficient, tissue necrosis results (Reuler & Cooney, 1981). The sites of most co~mon occurrence are the ssue over-lying the sacrum, ischia, and femoral trochanters (Peterson & Bittman, 1971; Richardson & Meyer, 1981; Roberts & Goldstone, 1979). These areas have also been found to be subject to high pressures in the lying and sitting positions (Kosiak, 1959; Linden, 1961) . Prevention of pressure ulcers is a problem unique to nursing. Other disciplines may investigate the causes of pressure ulcers, and physicians may prescribe programs for their treatment, but it is nurses who must provide the around-the-clock, day-to-day care that is required for their prevention. Recommendations for nursing interventions aimed at preventing pressure ulcers generally emphasize the importance of reducing the magnitude and duration of pressure application. These interventions are soundly based on scientific knowledge. However, a number of common nursing interventions are less soundly based on scientific knowledge. For example, massage of bony prominences is frequently mentioned in nursing textbooks as a preventive measure (Beland & Passos, 1975, 3 p. 889; Beyers & Dudas, 1977, p. 1130, Brunner, Emerson, Ferguson & Suddarth, 1970, p. 170; Brunner & Suddarth, 1974, p. 22; Martin, 1971). The use of heat lamps is common in the prevention and treatment of pressure ulcers. A common rationale stated by nurses is that their use increases local circulation, although this has not been documented in the research literature. The contribution of an impaired baseline local circulation to the development of pressure ulcers is unknown. Little information available regarding the normal circulation of areas susceptible to pressure ulceration. The most common type of study has utilized measurement of skin temperature to estimate changes in skin blood flow. A reactive hyperemia has been observed following the application of pressure in these areas (Goller, Lewis & McLaughlin, 1971; Mahanty & Roemer, 1979; Verhonick, Lewis & Goller, 1972). The 4 skin temperature of areas susceptible to pressure ulcers has been found to be lower than that of adjacent areas. However, variations in skin temperature are due to a number of factors other than local blood flow, including the metabolic rate of underlying tissue and the thermal conductivity of that tissue (Mahanty & Roemer, 1980). Since areas susceptible to pressure ulceration consist of a layer of skin with little underlying muscle or subcutaneous tissue, it is possible that the temperature variations observed are due not to variations in local circulation, but to variations in heat production by metabolism. Additional studies utilizing other methods of measuring skin blood flow in areas susceptible to pressure ulceration have yielded incomplete and contradictory evidence (Holloway, Dalt, Kennedy & Chimoskey, 1976; Larsen, Holstein & Lassen, 1979). If those nursing interventions aimed at preventing pressure ulceration by stimulating local circulation are to be based on scientific knowledge, the circulation of these areas must be studied. Further comparison of these findings with information regarding the local circulation in areas not prone to pressure ulceration would aid in the determination of a scientifically based nursing intervention. Baptista (1970) has described a simple thermal method for studying skin circulation. In the "thermal recovery method," cold is applied to the area of interest and the rate at which the skin temperature returns to normal is measured. This rate is an index of the circulation of the skin, and has been favorably compared with clearance of radioactive xenon as a method of studying skin circulation (Tavares, Farreta & Fernandes, 1975). The purpose of this study was to determine if there a difference between the cutaneous blood flow of areas prone to pressure ulceration, and adjacent, less susceptible areas, as measured by the thermal recovery method. Review of the Literature A number of factors including malnutrition, old age, obesity, circulatory deficiency, chronic illness, anemia, blood dyscrasias, skin ability, motor or sensory deficit, shear forces, f ction, edema, and pressure have been suggested as contributing factors in the development of pressure ulcers (Argis & Spira, 1979; Griffith, 1963; Isiandinso, 1979; Schell & wolcott, 1966; Williams, 1972). Only pressure has been consistently shown to cause ulceration, but some evidence suggests that friction (Dinsdale, 1974) and 5 shear force (Bennett, Kavner, Lee & Trainor, 1979; Palmer, 1979) also playa role in the development of pressure ulcers. Effects of Pressure on the Etiology of Pressure Ulcers The vast majority of research on the etiology of pressure ulcers has focused on the effects of exter-nally applied pressure. Experiments have been carried out utilizing isolated tissue and enzymes, unicellular organisms, animals, as well as human subjects. Isolated tissues and and unicellular 6 organisms. Cattell (1936) carried out experiments with isolated tissue, enzymes, and unicellular organisms in an attempt to determine if any physiologic effects could be produced as the result of pressure alone. Pressures in excess of 250,000 pounds per square inch were, at times, required to produce changes in cellular function. Since pressure alone cannot be responsible for cellular necrosis, a less direct effect must be responsible. Further research has led to the basic assumption that pressure ulcer formation is due to compression of capillaries by externally applied pressure, resulting in tissue anoxia, deprivation of nutrients, and accumulation of cellular waste products, leading eventually to tissue death (Dinsdale, 1973; 7 Kosiak, 1961; Trandel, Lewis & Verhonick, 1975). Animal studies. Because of the obvious ethical problems associated with producing pressure ulcers in human subjects, many studies of the etiology of pressure ulcers utilize animals. Brooks and Duncan (1940) applied pressure to rats' tails and found that the development of pressure ulcers was dependent on both the magnitude and duration of pressure application. This finding has been substantiated by a number of researchers (Daniel, Priest & Wheatley, 1981; Dinsdale, 1973; Kosiak, 1959). Hussain (1953) studied mouse tissue microscopically after the application of pressure, and found changes similar to those in tissues deprived of their blood supply_ These findings support the hypothesis that pressure interrupts the blood supply, causing pressure necrosis. Kosiak (1959) produced pressure ulcers in dogs by both the application of high pressure for short periods of time and application of lower pressure for long periods of time. The time pressure relationship was inverse and followed a parabolic curve. Microscopic changes indicative of anoxic necrosis were found in tissues subjected to as little as 60 mmHg pressure for as short a period of time as one hour. Kosiak (1961) also applied pressure to the ham- string muscles rats, and found a marked susceptibility of tissue to application of moderate pressure for relatively short periods of time. Tissue was less susceptible to alternating pressure than to constant pressure. 8 In another study (Daniel et al., 1981) pressure was applied over the femoral trochanters of swine. Tissue was found to be more resistant to pressure alone than previously thought, but friction combined with pressure greatly increased the susceptibility of tissue to ischemic necrosis. Muscle was found to be more susceptible to pressure ulceration than skin. These studies indicate that pressure ulcer formation is dependent on both the magnitude and duration of pressure application, and that reI f of pressure for short periods is protective. Although muscle is more susceptible to pressure induced ischemia than skin, pressure ulcers are primarily a problem of the skin, for a number of reasons. Necrosis of underlying muscle may produce no external signs. A force applied to the surface of the body leads to a cone shaped pressure gradient, with the force becoming spread out, and less pressure being applied to deeper layers of tissue (Nola & Vistnew I 1980; Reuler & Cooney, 1981). As long as the skin remains intact and maintains its function as a barrier, infection even of necrotic underlying tissue is unlikely. However, when the skin is broken, infection, sepsis, and death may result. Human studies. Studies of the etiology of 9 pressure ulcers in humans have been confined to measurement of capillary pressure, observation of the distribution of pressure over the surface of the body, epidemiological studies, and measurement of skin blood flow. Landis (1930) utilized the microinjection method to determine the capillary pressure in the base at the skin of the fingernail, and found the mean pressure in the arteriolar limb to be 32 mmHg. Other researchers (McClellan, McClellan & Landis, 1942), using pressure plethysmography, found capillary pressure in the forearm to range from 16-33 mmHg. The minimum pressure required to produce pressure ulcers is greater than the capillary pressure, supporting the hypothesis that pressure occludes capillary flow. Kosiak (1958) measured the pressures under the ischial tuberosities of subjects in the sitting position, and found it to exceed 300 mmHg when the subject was sitting on a flat, unpadded surface. Linden (1961) measured the distribution of pressure over the surface of subjects in the supine, prone, and lateral recumbent positions. In the supine pos 10 tion, he found the pressure applied to the sacrum was 60-70 mmHg. In the lateral recumbent position he found pressures of 70-95 mmHg applied to the hip, and in the sitting position, pressures of 65-100 rnmHg over the ischial tuberosities. A number of investigators (Peterson & Bittman, 1971; Richardson & Meyer, 1981; Roberts & Goldstone, 1979) have observed the incidence of pressure ulcers in various parts of the body. They found that pressure ulcers occur most frequently over the sacrum, ischia, and trochanters. The highest pressures are generated over the sacrum, trochanters, and ischia. These pressures exceed capillary pressure. Pressure ulcers occur most frequently at these sites. Based on these findings, it can be inferred that when pressure is applied to the surface of the body in sufficient magnitude, that pressure is transmitted to the underlying capillaries. If the transmitted pressure exceeds capillary intraluminal pressure, the capillaries collapse, interrupting the blood supply. If this pressure is prolonged, anoxic necrosis of tissue results, forming a pressure ulcer. Interruption of the pressure for short periods is protective, to a degree. 11 Skin Circulation Research indicates that pressure ulcers are caused by interruption of capillary blood flow to the skin. However, little information is available regarding the normal or pressure-altered skin blood flow in areas prone to pressure ulceration. Because of the role of the skin vasculature in blood pressure control and heat regulation, the vasculature of the skin is far more extensive than the nutritional needs alone of the skin would require (Ryan, 1976). The skin is supplied with an extensive network of vessels with great variety and density, and many anastamoses at all levels (Montagna & Prakkal, 1974). This great complexity, as well as variations between individuals, and in the same individual with advancing age has created difficulties in studying skin circulation (Ryan, 1976). Consequently, little information is available regarding the local cutaneous circulation of areas susceptible to pressure ulceration. Perforator arteries are the primary source of blood supply to the skin. These vessels pass through muscle, give off vessels to the muscles, and continue to the skin. A few direct cutaneous vessels also pass through muscle without giving off branches. Techniques for Measurement of Skin Circulation A number of techniques have been utilized in the study of the circulation of the skin. The skin circulation of areas prone to pressure ulceration has been studied by microscopic examination of tissue, clearance of radioactive markers, and various thermal methods. Because so little is known about the circu-lation of areas prone to pressure ulceration, it is appropriate and necessary to examine the methods used to study skin circulation. 12 Microscopic examination of the vessels in tissues subjected to a pressure load has been used to observe circulatory changes associated with pressure ulceration. Since this method involves producing a pressure ulcer and then removing a slice of tissue for examination, it is used only in animals. This method also does not provide information about the dynamic changes in skin blood flow that accompany application of pressure. Two invasive methods are frequently used to study skin blood flow. Systemic injection of fluorescein dye and observation of the resulting fluorescence has been used to study skin circulation (Ryan, 1973). Two days are required for clearance of the dye, and allergic reactions occur. Use of this method to study the skin circulation in relation to the etiology 13 of pressure ulcers has not been reported in the literature. Another invasive method involves measuring the rate of clearance of radioactive substances from an intradermal depot. 133xe and 131r -antipyrine have been injected into the skin and their rate of clearance measured by a radiation detection device in the study of pressure ulcers (Holloway et al., 1976; Larsen et al., 1979). The equipment for this measurement is expensive and inconvenient to use, and special precautions are required for handling of radioactive substances. The intradermal injection may also increase blood flow and thus distort flow values (Holloway, 1980). A wide variety of noninvasive measurement techniques have been used to study skin blood flow. Plethysmography records changes in volume and requires enclosure of the area of study (Ryan, 1976). This method is not adaptable to study of areas prone to pressure ulceration because the area of interest cannot be isolated. Laser doppler velocimetry has been used to estimate skin blood flow. The doppler shift produced in a beam of laser light by the movement of red blood cells is measured (Holloway & Watkins, 1977). Although this instrument is sensitive, reliable and convenient for clinical use, it is expensive and not readily available. 14 A readily available, inexpensive, and clinically useful method of estimating skin blood flow is measurement of skin temperature. Temperature is the degree of intensity of heat. Although temperature can be qualitatively sensed by receptors in the skin, its quantity cannot actually be measured. Changes in the physical properties of elements such as the volume of a gas, the pressure of a gas, the length of a piece of metal, or the electrical properties of a metal, occur with changes in temperature and can be used to provide quantitative measures of temperature (Mackay, 1970). The only instruments capable of detecting small, rapid changes in skin temperature are electrical thermometers. There are several types of electrical thermometers, including radiation thermometers, resistance thermometers, thermocouples, and thermistors. Radiation thermometers, also called thermographs, measure a portion of the infrared spectrum emitted by the body surface and transform it into a pictoral display (Verhonick et al., 1972). Thermography is usually used to determine temperature patterns in the skin and not for quantitative measurements of 15 small, rapid changes in skin temperature. Thermocouples and thermistors are attached directly to the surface of the skin and are capable of quanti-ly measuring small rapid changes in temperature. These probes do not actually measure the temperature of the skin but indirectly reflect the temperature of a probe in contact with the skin. The temperature of the probe must be allowed to equalize with the skin temperature before it can provide an accurate reflection of the skin temperature. Thermocouples measure the electromotive force generated by the junctions of two dissimilar metals at different temperatures. The probes are suitable for the measurement of core or skin temperature (Stoll & Hardy, 1950). Thermistors measure temperature changes indirectly by measuring the changes in resistance that occur in heavy metal oxides in proportion to changes in temperature. As the temperature of the thermistor increases, its resistance decreases, following a logarithmic curve. A minute amount of current passed through the thermistor, and changes in resistance are measured by determining the amount of current passing through a galvanometer. Since the temperature-resistance curve is not linear, the galvanometer used with the thermistor 16 requires a nonlinear scale. This difficulty can be overcome by constructing a bridge circuit in the instrument to compensate for the nonlinear relationship. Thermistors have a large change in resistance with relatively small changes in temperature, a rapid response time, and are relatively inexpensive. The disadvantages of thermistors include instability (their res tance gradually increases with age) and the need to recalibrate when thermistors (or thermo-meters) are changed (Krog, 1962). Simple measurement of skin temperature has been used frequently to estimate skin blood flow in pressure ulcer research (Barton, 1973; Goller, Lewis, McLaughlin & Verhonick, 1971; Howell, 1981; Mahanty & Roemer, 1979; Newman & Davis, 1981; Trandel, Lewis & Verhonick, 1975; Verhonick et al., 1972). If environmental factors are constant, skin temperature is dependent on the rate of skin blood flow, the temperature of the blood, the metabolic rate (and heat production) of underlying tissue, and the thermal conductivity of that tissue (Mahanty & Roemer, 1980). In the healthy human, blood temperature does not change signi antly during the period required for most blood flow measurements. The thermal conductivity of tissue at a given site is constant. In the resting 17 subject the metabolic rate of unstressed tissue remains relatively constant. Therefore, observations of temperature changes at the same unstressed site are probably relatively reliable indicators of changes in skin blood flow. However, simple measurement of skin temperature is a much less reliable method of measuring differences in skin blood flow of different areas of the body. The thermal conductivity and metabolic rate of underlying tissue vary greatly from site to site. The metabolic rate of muscle higher than that of skin (Nola & Vistnew, 1980). Therefore, the skin temperature of sites with underlying muscle will be warmer than that of sites with little or no underlying muscle. Thermal Method One thermal method of determining skin blood flow that overcomes the problem with simple thermometry has been described by Baptista (1970). In the "thermal recovery method," cold is applied to the skin in the area of interest, and the rate at which the skin returns to its normal temperature is measured. The time required for recovery to the original skin temperature is an index of the peripheral blood flow in the region studied. Baptista described the peripheral blood flow circulatory index (PBCI) as the time re- quired for the skin temperature to return half way to its original value, and cted that it would be smaller when the blood flow rate was greater. Since this method is less sensitive to variations in local metabolism than simple thermometry, it is a better measure of local circulation. This method is simple, noninvasive, and inexpensive. The thermal recovery method has been favorably compared with clearance of radioactive xenon as a method of studying skin circulation (Tavares et al., 1975). Both methods were used to measure the local circulation in the lower legs of three groups of subjects: normal subjects, hyperthyroid subjects with elevated skin temperature, and patients with presumably low cutaneous circulation (hypothyroid patients and those with obstructive atherosclerosis) . The mean blood flow values were determined each group and compared to the mean of the normal group for each method. The significance of difference of means was determined. For the thermal recovery 18 method, the values between normal subjects and those with hypocirculation were: ~=3.36, E< 0.001; between normal subjects and those with hypercirculation: t=4.04, E< 0.0001. For the xenon clearance method the values were: between normal and hypocirculation: !=3.98, 19 E< 0.0001; and between normal and hypercirculation: ~=2.33, E<O.Ol. The authors conclude that the thermal recovery method is more sensitive for studying skin hypercirculation, and less sensitive than xenon clearance for studying skin hypocirculation. The cold applied in the thermal recovery method may cause local vasoconstriction and increase the viscosity of the blood locally (Dodd, 1979). However, because of the relatively short period of time the cold is applied (one minute) these effects are probably minimal. The thermal recovery method is not a method of directly measuring skin blood flow, but measures the skin's ability to respond to the application of cold. Since the ability of the skin to respond to the application of cold is dependent primarily upon its circulatory capacity, the thermal recovery method is a good method of estimating local circulation. Changes in Skin Circulation Associated with Pressure Ulceration Some of these methods of investigating skin circu-lation have been used to determine the changes in circulation that are associated with pressure ulcer formation. These studies have contributed to the understanding of the etiology of pressure ulcers. However, the contribution of baseline differences in local skin circulation to the development of pressure ulcers is not known. 20 Some investigators have examined vessels microscopically following the application of a pressure load. Hussain (1953) applied pressure to rats' legs, and described a reactive hyperemia, edema, and frequently capillary and venous hemorrhage in the affected area following the release of pressure. He also showed that it was at this stage that the permeability of vessel walls increased, and localization of particulate matter, such as bacteria, occurred. Linden (1961) observed rabbits' ears following the application of pressure, and found a reactive hyperemia, followed by edema, dilatation of blood vessels, and extravasation of blood elements. Vascular changes lasted up to 12 days following removal of pressure that did not produce an ulcer. Dinsdale (1973) produced experimental ulcers in swine, and observed the formation of erythrocytic thrombi, followed by fibrin thrombi in venules and capillaries. He also noted changes in the ultrastructure of the capillaries. Barton (1973) examined mouse tissue that had been subjected to pressure and found a partial separation of endothelial cells. He felt that trauma could then 21 cause the cell junctions to break easily, exposing the blood to subendothelial tissue, and causing occlusion of the vessels by platelet thrombi. These studies suggest that changes 1n vascular structure resulting from pressure contribute to ulcer-ation by prolonging the period of decreased circulation after pressure is removed. Ho\...,ever, other methods of studying skin blood flow are needed to study the dynamic changes that occur when pressure is applied to tissue. One research group (Larsen et al., 1979) measured the "blood flow cessation external pressure" which is the pressure required to prevent the washout of an intradermal depot of ~133-antipyrine, in the sacral and T lumbar skin of human subjects. They found that the FeEP correlated strongly with the mean brachial arterial pressure, and was in the range of 63-138 rnrnHg. These findings could be interpreted to support the assumption that higher external pressures are required to produce pressure ulcers in hypertensive patients. A corollary of this assumption would be that hypotension increases the risk of pressure ulcer formation. This corollary is supported by this investigator's observation that hypotensive patients develop pressure ulcers with high frequency. Larsen et al. (1979) also found no significant dif 22 ference between the FCEP of sacral and lumbar skin. Thev interpreted this finding as evidence that local circulatory differences are not responsible for pressure ulcer formation, apparently because few pressure ulcers develop in the lumbar region. The sacral and lumbar regions both have relatively thin layers of muscle and subcutaneous fat between skin and underlying bone. Since the vasculature of the skin is primarily derived from the underlying muscle, it is likely that the skin vasculature of these areas is similar. An area with substantial layers of intervening muscle would likely have a different skin vasculature. Comparison of the skin circulation of an area prone to pressure ulceration with little underlying muscle with an area with substantial underlying muscle would probably yield more valuable information regarding the contribution of local differences in circulation to the development of pressure ulcers. Another group of researchers (Holloway et al., 1976) utilized clearance of xe 133 to compare the skin circulation of the sacrum and forearm. They found that lower pressures were required to occlude capillary flow in sacral skin than in forearm skin. These findings could be used to support the assumption that local skin circulatory differences do contribute to the 23 development of pressure ulcers. However, the forearm and sacrum are vlidelv separated areas, and factors other than local circulatory differences could intervene. It is also probable that the varying amounts of padding between the two areas cause greater pressures to be transmitted to the capillaries of the sacral skin. These studies do not measure the baseline circulation, but the ability of the circulation to function under a pressure load. Studies using clearance of radioactive substances to study skin circulation of areas prone to pressure ulceration are incomplete and contradictory. A number of studies have utilized skin temperature measurement to estimate skin blood flow in relation to pressure ulcer formation. In one study (Goller et al., 1976) pressure was applied to human skin and the skin temperature was measured with thermography following the release of pressure. An increase in temperature was noted following release of pressure. In another study (Verhonick et al., 1972) pressure was applied to the body surface by having the subject lie on the area to be studied, and skin temperature was measured thermographically after pressure was removed. An initial cooling at the highest pressure point was noted, followed by a "flushing" to a temper- ature above normal, and then a return to the normal temperature stribution. Mahanty and Roemer (1979) applied pressure over the femoral trochanters of six young human subjects and measured the skin temperature with thermocouples after the pressure was released. They found an increase in skin temperature that was directly proportional to the amount of pressure and the length of time it was applied. Newman and Davis (1981) obtained thermographs of 24 the ischial and sacral areas of hospitalized atric patients after a load had been applied by having the patient lie on the area to be studied. They found that patients who demonstrated a "thermal flare" after pressure had been released were more prone to pressure ulcer formation. The initial cooling observed by Verhonick et ala is probably due to evaporative cooling. Moisture on the surface of the body would not evaporate while the subject was lying on the area of study. When the area was exposed for thermography, evaporative cooling could occur. The increase in temperature observed following release of pressure can be explained by the mechanism of reactive hyperemia. After blood flow is occluded 25 by pressure, and then reestablished by the release of pressure, circulation to the area is increased as a compensatory mechanism. Lewis and Grant (1925) and Goldblatt (1926) studied reactive hyperemia in man, and found that it was a local reaction, independent of central nervous system and hormonal control. It occurred whenever the arterial supply was occluded, and was characterized by vasodilatation. The extent and duration of the reactive hyperemia has been found to be proportional to the local metabolic debt (Lewis & Landis, 1929). By this mechanism, tissue temporarily deprived of its blood supply is protected from necrosis. The skin temperature of subjects lying on a transparent surface was measured in another study (Trandell et al., 1975) by obtaining thermographs of the subjects taken through the transparent surface. Areas prone to pressure ulceration, which were also exposed to the highest pressures, were found to have the highest skin temperature. One would expect that the areas subjected to the highest pressure would have decreased skin blood circulation and lower skin temperatures. The authors offered no explanation for this seemingly contradictory finding. Since the areas that were subjected to the highest pressures were in closest contact with the transparent surface, heat loss in these areas was probably minimal. It is likely that in this study, the increased skin temperature was not due to increased circulation but rather to decreased heat loss. 26 Howell (1981) measured the skin temperature of elderly, ambulatory, ulcer-free females over the trochanters, sacrum, heels, and lateral malleoli, and compared these temperatures to the skin temperature of adjacent areas not prone to pressure ulceration. He found that areas prone to pressure ulceration were cooler than the adjacent areas. Howell explained the cooler skin temperatures of areas prone to pressure ulceration as being due to decreased circulation in these areas. However, areas prone to pressure ulceration are characterized by very little or no underlying muscle or bone (Nola & vistnew, 1980). Therefore, the differences in temperature may be due to increased heat production by muscle in the less susceptible areas rather than differences in skin circulation. These studies of the local circulation in relation to pressure ulcer formation showed that changes in the ultrastructure of the vasculature occur following application of pressure, at least in animal studies. A reactive hyperemia has been shown to occur following the release of pressure. Very little research has been conducted to study the baseline circulation of areas prone to pressure ulceration. Since the skin vasculature is derived from underlying muscle, areas prone to pressure ulceration may have a decreased circulation. The evidence of whether circulation in these areas is decreased is incomplete and contradictory. Summary Because of the obvious ethical problems of deliberately producing pressure ulcers in human subjects, much of the basic research on pressure ulcers has been done with animals. Animal studies have 27 shown that pressure ulcers are produced by externally applied pressure which causes occlusion of the capillaries, and results in tissue necrosis. The development of pressure ulcers has been shown to be dependent on both the magnitude and duration of pressure application. Microscopic changes in the vasculature of skin have been observed following the application of pressure. Human studies have shown that pressure ulcers develop most commonly in areas that are subject to the highest pressure, primarily the sacrum, hips, and ischia. Little information regarding the local circulation of areas susceptible to pressure ulceration is avail- able. Two studies utilizing the clearance of radioactive substances showed that skin blood flow ceases 28 at pressures thought to be capable of producing pressure ulcers, but the data is incomplete and contradictory. Studies utilizing thermometry as a means of studying local skin circulation in these areas have recently become quite popular. These studies have shown that areas prone to pressure ulcer formation demonstrate increased temperature after a pressure load is applied. Other skin temperature studies have shown that areas prone to pressure ulcer development are cooler than adjacent areas. Since skin temperature is dependent on metabolic rate as well as the rate of blood flow, the question of whether decreased baseline local blood flow contributes to the development of pressure ulcers has not been answered. The thermal recovery method is a simple, noninvasive method of estimating local skin blood flow, and is less sensitive to metabolic differences than simple thermometry. Thermistors are an appropriate means of measuring skin temperature. CHAPTER II CONCEPTUAL FRAMEWORK Assumptions The following assumptions were used in formulating a conceptual framework for this study: 1. Pressure ulcers are areas of hypoxemic necrosis caused by compression of capillaries by externally applied pressure. 2. If the skin blood flow is decreased, a less severe pressure load is required to compress the capillaries and cause pressure ulceration. 3. The skin blood flow varies from one area of the body surface to another. Decreased skin blood flow may be a contributing factor to the high inc dence of pressure ulceration in certain areas of the body. 4. The rate at which cooled tissue is rewarmed is a function of local skin blood flow. Framework Pressure ulceration is due to compression of the capillaries by externally applied pressure, resulting in interruption of blood flow and hypoxemic necrosis. When the pressure applied to the capill exceeds capillary intraluminal pressure, the capillaries are compressed and blood flow decreases. If llary intraluminal pressure is decreased, less external pressure is required to interrupt blood flow. Capil-pressure is determined by flow and resistance. When the flow through the capillaries is capil intraluminal pressure is decreased. Thus, when skin blood flow is decreased, a less severe sure load is required to interrupt flow, and the k of pressure ulceration is increased. Skin blood flow in certain areas of the body may be less than in other areas. These areas would be at greater risk of deve ng pressure ulcers. Pressure ulcers develop most frequently over the ischia, trochanters, and sacrum. The sacrum and trochanters have very little muscle between skin and underlying bone. The vasculature of the skin is derived from underlying muscle. Therefore, the skin blood flow in these areas may be decreased. This decreased blood 30 flow would contribute to the development of pressure ulcers in these areas. Determination of any differences between skin blood flow of these areas and other areas not prone to pressure ulceration, will contribute to 31 understanding of the etiology of pressure ulceration. A number of techniques exist for measuring skin blood flow. Most of these techniques involve the use of expensive equipment that is not readily available. Measurement of skin temperature is a technique for estimating skin blood flow that requires less-expensive, more readily-available equipment. However, skin temperature is affected by factors other than blood flow, including metabolic rate of underlying tissue. If cold is applied to the surface of the body, heat moves from the warmer area (the body) to the cooler area (the cold applicator). After the cold applicator is removed, the area to which it was applied is cooler than the surrounding tissue. Heat again moves from the warmer area to the cooler area. Blood is warmer than the cooled area. If a large amount of blood moves quickly to the cooled area, heat will be trans more quickly than if a small amount of blood moves sluggishly to the cooled area. Therefore, the time required for thermal recovery of tissue is a function of the circulatory capacity of the tissue. The skin circulation can be estimated by applying cold to the skin and measuring the rate at which its temperature returns to the original value. A more rapid recovery indicates that the skin blood flow is greater, while a slower recovery indicates that the skin blood flow is less. The purpose of this study was to determine if 32 the skin blood flow, as measured by the thermal recovery method, is decreased in areas prone to pressure ulceration such as the sacrum and trochanters, when compared with adjacent, nonsusceptible areas. Research tions The specific research questions to be answered in this study were: 1. Is the peripheral blood flow circulatory index (PBCI) over the trochanter significantly higher than the PBCI over the groin? 2. Is the PBCI over the sacrum significantly higher than the PBCI over the abdomen? Definitions The following operational definitions were utilized in the study: 1. Peripheral blood flow circulatory index: The time required for the skin temperature to return half way to its original value following the application of cold. 2. Trochanter: The area of body surface des- cribed by a circle ten centimeters in diameter, with its center over the palpated femoral trochanter. 3. Groin: The area of body surface described by a circle ten centimeters in diameter, with its center midway between the anterior superior iliac spine and the symphysis pubis. 4. Sacrum: The area of body surface described by a circle ten centimeters in diameter, with its 33 center over the most prominent palpated sacral tubercle. 5. Abdomen: The area of body surface described by a circle ten centimeters in diameter, with its center midway between the xyphoid process and the umbilicus. 6. Right brachial region: The area of body surface described by a circle ten centimeters in diameter centered over the biceps muscle on the right arm. 7. Experimental sites: A randomly selected trochanter, the ipsilateral groin, the sacrum, and the abdomen. 8. Control sites: The contralateral groin and the right brachial region. 9. Skin temperature: Expressed in degrees centigrade, measured by skin thermistors attached to the sites of interest, and displayed on an electronic thermometer. CHAPTER III METHODOLOGY AND RESEARCH DESIGN Aim The aim of this study was to determine if skin blood flow, as measured by the thermal recovery method, is less in areas susceptible to pressure ulcers than in adjacent, nonsusceptible areas. Skin circulation was measured over the trochanter and sacrum, and compared with the skin circulation measured over the groin and abdomen. This information will contribute to understanding of the etiology of pressure ulcers and ultimately to determining appropriate nursing care for their prevention and treatment. Population The study population consisted of a convenience sample of 30 subjects selected from a geriatric health screening center staffed by health science students from the University of Utah. The center offered a number of services including blood pressure screening, hematocrit and blood glucose testing, nutritional 35 counseling, pedicures, cerumen removal, and physical examinations. Subjects were recruited from clients utilizing these services. Subjects were approached in the waiting area and after a brief explanation, were asked if they would be willing to participate in the study. Subjects who met the following criteria were asked to participate in the study: 1. At least 60 years of age. 2. Willing to sign the consent form. 3. Willing to cooperate with the measurement procedures for about 45 minutes. 4. No history of diabetes mellitus or serious skin disorders. 5. Lack of current pressure ulcers or skin disorders. Design The design of this study was descriptive. All thermal recovery measurements were made under similar conditions on all subjects. Each subject served as his/her own control. Instruments All instruments used for data collection were noninvasive. All measurements were made by the investi- 36 gator. Thermometers Two Digitec electronic thermometers with mUltiple monitoring channels (Model 5810) and Yellow Springs Instrument thermistor button probes were used to measure skin temperature. The thermistors were held in place on the skin with paper tape and were insulated with a cotton ball (Appendix B details instrument specifications) . Cold licators Two glass containers, each with a diameter of ten centimeters and filled with a slurry of ice and water, were used to apply cold to the skin. A plas wrap was placed over the opening of the container and held in place with an elastic band to prevent spillage. Skin Marker A water soluble marking pen was used to mark the skin for application of cold and placement of thermistors. A glass container identical to those used to apply cold was used as a template to mark circles ten centimeters in diameter. Sphygmomanometer and Scales Blood pressure was measured from the right arm with a mercury sphygmomanometer and a stethoscope, using the standard procedure (Kirkendall, Burton, Epstein & Freis, 1967). Weight was measured on a balance scale. Height was measured with a ruler attached to the scale. Room Thermometer Room temperature was measured before and after thermal recovery measurements on each subject, using a mercury-in-glass thermometer (Springfield No. 096). Data Collection Procedures Assignment of Experimental and Control Sites Because of the pressure load created by the sub-ject lying on an area of study is known to alter skin blood flow, areas not subjected to a pressure load were studied. were randomly assigned to two 37 groups of equal size. In one group of 15, subjects were asked to lie on their left side, and the right tro-chanter and groin were studied. In the other group of 15 subjects, they were asked to lie on their right side, and the left trochanter and groin were studied. The study occurred in two phases. During the first phase, the thermal recovery method was used to study the exposed trochanter and the ipsilateral groin. To control for changes in temperature due to 38 environment, measurement, or physiologic factors, skin temperature was recorded at 20-second intervals over the contralateral groin and right brachial region. During the second phase of the study, the thermal recovery method was used to study the sacrum and abdomen. Skin temperature was measured over the right brachial region at 20-second intervals to serve as a control during the second phase of the study. Data Record Data were recorded by hand on a data collection sheet (Appendix C). Skin temperature was recorded at two experimental (trochanter, ilateral groin) and two control (contralateral groin, right brachial region) sites during the first phase of the study. Skin temperatures were recorded at two experimental (sacrum and abdomen) and one control site (right brachial region) during the second phase of the study (Figure 1). Two e ronic thermometers, each with three channels were used, and manual switching was required. The same thermistors and thermometer channels were used at each s Baseline skin temperature was recorded at all sites five minutes after application of the thermistors. The cold glass container was then applied to the experimental sites for one minute. Following appli- Contralateral Groin Right Brachia Region Figure 1. . Trochanter Ipsilateral Groin Experimental and control sites. 39 40 cation of cold, skin temperature was recorded at 20- second intervals, as determined by the sweep hand on a wristwatch. Skin temperature measurements were recorded until the skin temperature had returned half-way to the baseline skin temperature. Determination of the Peripheral Blood Flow Circulatory Index (PBCI) The PBCI is the index of skin circulation of the thermal recovery method. It is the time required for the skin temperature to return halfway to the baseline temperature following the application of cold. In order to calculate the PBCI the following procedure was used: 1. Subtract the lowest skin temperature following the application of cold (Tc) from the baseline skin temperature (Tb ). This value is the initial decrease in skin temperature. 2. Divide the initial decrease ln skin temperature by two. 3. Add the resulting figure to the lowest skin temperature following the application of cold (Tc ). This value is the temperature midway between the baseline skin temperature (Tb ) and the lowest skin temperature following the application of cold (Tc) and is termed the calculated T~. The formula for calcu- 41 lation of the calculated T~ is: 4. Compare the calculated T~ to the recorded skin temperature values. Since skin temperatures were recorded at 20-second intervals, the calculated seldom corresponds exactly to recorded values. If the calculated T~ is between two recorded values, the time at which the lower of the two recorded values was measured is the PBCI. Therefore, the accuracy of this measurement is + 19 seconds. Overview of Data Collected Demographic data including sex, age, weight, height, blood pressure, medications taken, and medical history were collected on each subject. Room tempera-ture was recorded at the beginning and end of the data collection period. During the first phase of the study, a baseline temperature was recorded for the experimental sites (exposed trochanter and ipsilateral groin) and the control sites (contralateral groin and right brachial region) . Skin temperatures of these four sites were recorded immediately following the application of cold to the trochanter and ipsilateral groin, and at 20-second intervals thereafter. Skin temperatures continued to 42 be recorded until skin temperature had returned half - way to the baseline temperature. During the second phase of the study, baseline skin temperatures were recorded at the experimental sites (sacrum and abdomen) and at the control site (right brachial region). Following application of cold to the sacrum and abdomen, skin temperature measurements were recorded at all three sites, using the same procedure as during the first phase of the study (Appendix D lists the complete protocol) . CHAPTER IV DATA ANALYSIS Methods of Data Descriptive statistics about the mean, the paired ~-test, one-way analysis of variance, and the correlation coefficient were used to analyze the data. Calculations were completed using the Tektronix 4052 computer and statistical software. Descriptive Statistics The mean, standard deviation, and range were calculated for the following data: 1. The initial skin temperature at each experimental site (Phase one: trochanter and ipsilateral groin; Phase two: sacrum and abdomen) and each control site (Phase one: contralateral groin and right brachial; phase two: right brachial) . 2. Skin temperature at each experimental and control site for each 20-second measurement period following application of cold (descriptive statistics for skin temperature are listed in Appendix E) . 3. The PBCI for each experimental site (Phase one: trochanter and ipsilateral groin; Phase two: sacrum and abdomen) for all subjects. Paired t-Test 44 The t-test is the basic parametric procedure for testing differences between two group means. Since a single group of subjects was used, and subjects served as their own controls, the paired ~-test was used. This procedure is used for testing difference in the means of dependent groups (Polit & Hungler, 1978, pp. 548-551). The paired t-test was used to test for statistical differences between: 1. The initial skin temperature at all seven sites. 2. The initial decrease in skin temperature of the experimental sites. 3. The temperature of the control sites at the beginning and end of each phase of the study. 4. The PBels of the experimental sites. The ~-test for independent variables was used to test for statistical difference between: 1. The PBels of the left and right trochanters. 2. The PBels of male and female subjects. Because a directional hypothesis was proposed, a one-tailed t-test was used to determine the E values between the PBCls of the trochanter and groin, and between the PBCls of the sacrum and abdomen. The two tailed t-test was used in all other instances. Ana is of Variance 45 Analysis of variance (ANOVA) is a parametric procedure used to test the significance of difference between group means of more than two groups (Polit & Hungler, 1978, pp. 553-559). One-way, completely randomized, analysis of variance was used to test for statistical differences based on: 1. Subject age. 2. Height/weight ratio. 3. Diastolic blood pressure. Correlation Coefficients The most common method of describing statistical relationships between two measurements is the correlational procedure (Polit & Hungler, 1978, pp. 528- 533). This procedure was used to determine correlational relationships between: 1. The initial decrease in temperature and the PBCI at each site. 2. The PBCls of all four sites. The S Results of Data Ana is lation 46 A convenience sample of 30 subjects was obtained. All subjects were cl nts of the health screening center. Since these subjects were all relatively healthy, ambulatory, living at horne, and relatively well-informed and concerned about their health, they were probably representative of the majority of the elderly population. Sixteen females and 14 males participated in the study. The age of the subjects ranged from 60 to 87 years, with a mean age of 70.6 years (S.D. ~ 7.2). Twelve of the subjects were taking antihypertensive medications. Only two subjects had a diastolic blood pressure higher than 90 rnrnHg. The right trochanter and groin were subjected to the thermal recovery method in 15 subjects, and the left trochanter and groin were used in 15 subjects. One subject had a pressure ulcer during a hospitalization 20 years previously (Table 1). Environmental Conditions The study was conducted from May 10 to June 7, 1983. Measurement took place between one pm and fourthirty pm. Measurements on all subjects occurred in the same small (6x8 feet), unventilated room. During Table 1 Study Population Characteristics Subj. Sex Age Blood Weight Height Weight Height Trochanter Pressure (kg) ( em) Ratio (kg/em) Studied 1 M 62 134/74 80 173 0.46 R 2 M 68 140/84 57.2 163 0.35 R 3 M 75 128/68 68.2 170 0.40 R 4 M 67 150/84 56.8 168 0.34 R 5 F 85 136/84 56.8 163 o . 35 L 6 M 77 134/76 80 179 0.45 L 7 M 68 144/74 75 165 0.45 R 8 F 75 124/76 56.4 163 0.35 L 9 F 87 140/80 55.9 165 0.34 L 10 M 76 124/70 71.8 180 0.40 R 11 M 76 154/90 76.8 174 0.44 L 12 F 78 130/70 56.4 145 0.39 R 13 M 68 140/100 85 178 0.48 R 14 F 70 140/80 83.4 171 0.49 R 15 F 60 126/70 74.5 165 0.45 L 16 M 80 110/50 76.4 173 0.44 L .::::. -.J Table 1 (Continued) Subj. Sex Age Blood Weight Height ght Height Trochanter Pressure (kg) ( em) Ratio (kg/em) Studied 17 M 72 134/80 65 170 0.38 R 18 F 65 150/84 61.8 161 0.38 L 19 M 72 116/60 73.4 168 0.44 L 20 F 65 118/70 52.3 165 0.32 L 21 F 60 138/78 69.5 169 0.41 R 22 M 70 134/86 73.6 170 0.43 R 23 F 69 142/90 70.2 163 0.43 L 24 F 72 112/60 66.8 160 0.42 R 25 F 64 176/92 69.1 169 0.41 L 26 M 68 138/72 66.8 168 0.40 L 27 F 67 116/60 62.5 164 0.38 R 28 F 62 148/92 70.9 160 0.44 R 29 F 81 150/90 63.6 157 0.41 L 30 F 60 124/78 61.4 173 0.35 L Mean F=16 70.6 135/77 67.9 167 0.41 L=15 M=14 R=15 S.D. 7.2 14.5/11.3 8.9 7.1 ~ co 49 the study, room temperatures ranged from 24C C to 26° C, but did not vary during the course of measurement of anyone subject. Subjects wore hospital gowns and their underclothes. Subjects who wore LDS garments were asked to remove them. Subjects were covered with a sheet, and all stated they were comfortable in regard to temperature. None of the subjects shivered during the measurements. Skin Temperatures The baseline skin temperatures ranged from 29.5° C to 36.0° C (Table 2). The groins were the warmest areas. The groins were significantly warmer than the trochanter, sacrum, and abdomen. The trochanter was the coolest area. It was significantly cooler than the groin, sacrum, and right brachial regions (Table 3). The mean skin temperatures of the sacrum and abdomen were identical. Following application of cold, an immediate decrease in the skin temperature of the experimental sites (trochanter, groin, sacrum, and abdomen) was noted (Table 4). Skin temperatures frequently continued to decrease for one to four additional measurement periods (20-80 seconds). The skin temperature of the sacrum decreased significantly less than that of the trochanter 50 Table 2 Initial Skin Temperature (o C) Site Mean Standard Range Deviation Phase One Trochanter 32.7 1.28 29.4-36.0 Ipsilateral Groin 33.9 0.96 31.0-35.0 Contralateral Groin 33.9 1.16 31.4-35.5 Right Brachial 33.2 1.16 31.7-35.8 Phase Two Sacrum 33.3 1.22 30.6-35.3 ]\.bdomen 33.3 1.21 30.6-35.3 Right Brachial 33.9 1.12 31.1-35.3 Ipsilateral Groin Contralateral Groin Right Brachial #1 Sacrum Abdomen Right Brachial #2 Table 3 t-Statistics and £-Values: Initial Skin Temperatures Ipsilateral Contralateral Trochanter Groin Groin Brachial #1 Sacrum Abdomen t=-6.252024 2=0.0000 t=-5.87805 t=. 61380 E=O.OOOO £=.54410 t=2.07603 t=4.08l97 t=3.72367 £=.04688 .00032 £=.00084 t=2.90454 t=3.92976 t=3.l0304 t=0.32656 £=.00698 £=.00048 £=.00426 .74632 t=1.82247 t=3.43787 t=2.83449 t=.09639 t=.52788 .07872 £=.00180 £=.00828 £=.92386 £=.60158 t=-3.52534 t=.43882 t=.01654 t=2.25260 t=2.l8l99 t=2.3l33l £=.00142 £=.66402 .98692 £=.03204 £=.03736 £=.02800 V1 I--' 52 Table 4 Decrease in Skin Temperature (0 C) Following Application of Cold Site Mean Standard Range Deviation Trochanter 5.4 1.15 2.5-8.3 Groin 4.8 1.67 0.5-7.7 Sacrum 4.0 1.71 1.6-8.8 Abdomen 4.8 1.51 1.9-7.6 53 (:e.< 0.005) and the abdomen (:e.< 0.05). The skin temper-ature of the abdomen also decreased less than the temperature of the groin, but the difference only approached significance (:e.=.053). No significant differences were found between the temperature de-creases over the trochanter, groin, and abdomen (Table 5) • During the first phase of the study, while the thermal recovery method was being applied to the tro-chanter and groin, skin temperatures were recorded over the contralateral groin and the right brachial region as a control (Table 6). During phase one the mean skin temperature of the contralateral groin increased O. 3 o C (E < 0.001). The mean temperature of the right brachial region increased O. 59C C (:e. < 0 .001) . During the second phase of the study, while the thermal recovery method was being applied to the sacrum and abdomen, the skin temperature of the right brachial region was recorded as a control (Table 7). During phase two, the mean skin temperature of the right brachial region decreased 0.08° C (E=0.33). Peripheral Blood Circulatory Index (PBCI) The PBCI data were analyzed in relation to the research questions: 54 Table 5 t-Statistics and ~-Va1ues: Decrease in Skin Temperature Trochanter Groin Sacrum Groin t=1.47929 12:=.14984 Sacrum t=3.60812 t=2.01748 12:=.00114 12:=.05300 Abdomen t=1.69256 t=.20926 t=2.23643 12:=.10128 12:=.83578 12:=.03318 55 Table 6 Skin Temperatures at Experimental and Control Sites (Phase I) Right Trochanter Brachial Groin Baseline Mean S.D. After Cold Mean S.D. 32.7 1.28 27.4 1.34 (Control Site) 33.2 1.34 33.5 1.14 Change in Skin Temperature Between Baseline and Removal of Cold Mean S.D. E Baseline Mean S.D. -5.3 1.15 0.0000 32.7 1.28 At PBCI Time Mean S.D. 30.0 1.15 +0.3 0.06 0.002 33.2 1.34 33 .. 8 1.19 Change in Skin Temperature Between Baseline and PBCI Time Mean S.D. E -2.7 0.67 0.0000 +0.6 0.1 0.0004 33.9 0.96 29.1 1.55 -4.8 1.67 0.0000 33.9 0 .. 96 31.4 0.96 -2.5 0.58 0.0000 Contralateral Groin (Control Site) 33.9 1.16 34.0 1.14 +0.1 0.03 0.001 33.9 1.16 34.2 1.14 +0.3 0.1 0.0002 56 Table 7 Skin Temperatures at Experimental and Control Sites (Phase II) Right Sacrum Brachial Abdomen (Control) Baseline Mean 33.3 33.9 33.3 S.D. 1.22 1.12 1.28 After Cold Mean 29.8 33.7 28.7 S.D. 1.82 1.24 1.86 Change in Temperature Between Baseline and Application of Cold Bean -4.0 -0.2 -4.6 -S.D-. 1.7 0.03 1.5 12. 0.0000 0.29 0.00000 Baseline Mean 33.3 33.9 33.3 S.D. 1.22 1.12 1.28 At PBCI Time Mean 31.3 33.8 30.9 S.D. 1.28 1.24 1.37 Change in Temperature Between Baseline and PBCI Time Mean -2.0 -0.1 -2.4 S.D. 0.8 0.02 0.7 E 0.0000 0.33 0.0000 -.-~---.--.. - 1. Is the PBCI greater over the trochanter than over the groin? The mean PBCI over the trochanter was 277 seconds (S.D. ~ 93), and the mean PBCI over the groin was 261 seconds (S.D. ~ 81). This difference was not statis-tically significant ( . 2 3 ) ( Tab 1 e 8). 2. Is the PBCI greater over the sacrum than over the abdomen? The mean PBCI over the sacrum was 327 seconds (S.D. + 156), while the mean PBCI over the abdomen was 308 57 seconds (S.D. ~ 144). This difference was not statis-tically significant (E=. 30) (Table 9). Further analysis of the data showed no significant differences in the PBCIs of any sites based on sex (Table 10), age (Table 11), diastolic blood pressure (Table 12), or height/weight ratio (Table 13). No significant differences were found between the PBCIs of the right and left trochanters (Table 14). Correlation coefficients were calculated between the PBCIs of all the experimental sites (Table 15). A positive correlation was noted between the PBCI of the trochanter and the PBCI of the abdomen (E < 0.001) . The positive correlation between the PBCI of the sacrum and the PBCI of the groin approached signifi-cance (p< 0.1) . Correlation coefficients were calculated between Table 8 Peripheral Blood Circulatory Index Trochanter Groin Trochanter and Groin Mean 277 261 Standard Deviation 93 81 Range 120-560 80-800 58 0.23 Sacrum Abdomen Table 9 Peripheral Blood Circulatory Index Sacrum and Abdomen Mean 327 308 Standard Deviation 156 144 Range 80-800 100-780 59 0.30 60 Table 10 Two Sample t-test (Unequal Variance) PBCI Male and Female Male Mean Female Mean t- E- (n=14 ) (n=16) statistic value Trochanter 296 264 0.91 0.38 Groin 257 265 0.86 0.80 Sacrum 364 316 1.17 0.41 Abdomen 281 345 0.25 Table 11 ANOVA of PBCI by Age Sum of Site Source Squares df Trochanter Between Groups 730.000 2 Among Groups 251056.667 27 Total 251786.667 29 Groin Between Groups 8830.000 2 Among Groups 183556.667 27 Total 192386.667 29 Sacrum Between Groups 93926.667 2 Among Groups 608860.000 27 Total 702786.667 29 Abdomen Between Groups 51420.000 2 Among Groups 547460.000 27 Total 598880.000 29 Mean Square 365.000 9298.395 4415.000 6798.395 46963.333 22550.370 25710.000 20276.296 F - 0.039 0.649 2.083 1.268 Significance Level 0.963 0.527 0.142 0.294 0"\ I-' Table 12 ANOVA of PBCI by Diastolic Blood Pressure Sum of Mean Site Source Squares df Square Trochanter Between Groups 9266.667 3 3088.889 Wi thin Groups 242520.000 26 9327.692 Total 251786.667 29 Groin Between Groups 4386.667 3 1462.222 Within Groups 188000.000 26 7230.769 Total 192386.667 29 Sacrum Bet\.,reen Groups 65906.667 3 21968.889 ~vi thin Groups 636880.000 26 24495.385 Total 702786.667 29 A-bdomen Between Groups 14760.000 3 4920.000 Within Groups 584120.000 26 22466.154 Total 598880.000 29 F 0.331 0.202 o . 897 0.219 Significance Level o . 803 o . 894 0.455 0.882 0"\ N Table 13 ANOVA of PBCI by Height/Weight Ratio Sum of Mean Site Source Squares df Square Trochanter Between Groups 23895.758 3 7965.253 Within Groups 227890.909 26 8765.035 Total 251786.667 29 Groin Between Groups 7355.152 3 2451.717 vIi thin Groups 185031.515 26 7116.597 Total 192386.667 29 Sacrum Between Groups 51710.606 3 17236.869 Wi thin Groups 651076.061 26 2504.387 Total 702786.667 29 ]I.bdomen Between Groups 36775.758 3 12258.586 Within Groups 562104.242 26 21619.394 Total 598880.000 29 F 0.909 0.345 0.688 0.567 Significance Level 0.449 o • 793 0.566 0.641 0'\ W Table 14 Two Sample t-test (Unequal Variance) Mean Right Trochanter 269 PBCI Right and Left Trochanter Hean Left Trochanter 288 tstatistic 0.54 64 pvalue 0.59 65 Table 15 Correlation Matrix: PBCI Experimental Sites PBCI PBCI PBCI Trochanter Ipsilateral Sacrum Abdomen Groin PBCI Trochanter 1.00000 0.06749 0.20774 0.61455 PBCI Ipsilateral 0.06749 1.00000 0.31290 -0.15131 Groin PBCI Sacrum 0.20774 0.31290 1.00000 0.13540 PBCI Abdomen 0.61455 -0.15131 0.13540 1.00000 66 the initial decrease in skin temperature and the PBel at each site. A positive correlation was found between the initial decrease in skin temperature of the sacrum and the PBel of the sacrum (E< 0.02) (Table 16). Discussion Research has shown that pressure ulcers are caused by hypoxemic necrosis due to interruption of blood flow to the affected tissue. Areas that are frequently subjected to high pressure, such as the sacrum and trochanter, develop pressure ulcers with high frequency. Research conducted on the skin circu-lation of these two areas has shown that blood flow decreases during the application of pressure, and that a reactive hyperemia occurs following the release of pressure (Barton, 1973; Goller et al., 1976; Kosiak, 1959; Nola & Vistnes, 1980). The contribution of local differences in the baseline circulation of skin that has not been subjected to a pressure load to the development of pressure ulcers is unknown. In order to determine the contribution of local differences in skin circulation to the development of pressure ulcers, this study addresses two research questions: 1. Is the peripheral blood flow circulatory index (PBel) of the trochanter significantly greater than the PBel Table 16 Correlation Coefficients Initial Temperature Decrease versus PBCI Trochanter Groin Sacrum Abdomen -0.30 0.29 0.45 0.27 67 68 of the groin? No significant differences were found between the PBCls of these two sites. Since the PBCI reflects the rates of blood flow in these two areas, it is concluded that blood flow comparisons, as measured by the thermal recovery method, between the trochanter and the groin do not differ significantly. These findings are contradictory to earlier interpretations (Barton, 1973; Howell, 1981; Trandel et al., 1975) of skin temperature values. These researchers have assumed that the decreased skin temperature of areas prone to pressure ulceration is due to decreased blood flow in these areas. The results of the current study suggest that these skin temperature differences are not due to differences in skin blood flow. Areas prone to pressure ulceration usually consist of skin with relatively thin layers of underlying muscle or subcutaneous fat. Since muscle is metabolically more active than skin, it produces more heat than skin. It is probable that areas prone to pressure ulceration are cooler than other areas because less heat is produced by underlying tissue in these areas. This investigation speculated that areas of the body with decreased skin circulation, before a pressure 69 load is applied, require a less severe pressure stress for hypoxemic necrosis and ulceration to occur. It was further speculated that a contributing factor to the high incidence of pressure ulceration in certain areas of the body may be that the baseline skin cir-culation of these areas is decreased. The results of this study do not support this speculation. No sig-nificant differences were found between the PBCIs of the trochanter and groin. Therefore, decreased skin circulation when no pressure load has been applied does not appear to be a contributing factor to the high incidence of pressure ulceration over the tro-chanter. It is also possible that the thermal re-covery method, and skin temperature measurement tech-niques do not adequately reflect the state of the cutaneous circulation. 2. Is the PBCI of the sacrum significantly greater than the PBCI of the abdomen? No significant differences were found between the PBCIs of the sacrum and groin. As was the case with the trochanter and groin, researchers had assumed that the decreased skin temperature over the sacrum was due to decreased blood flow. The investigator speculated that decreased skin blood flow in skin which had not yet been subjected to a pressure load contributed to the high incidence of pressure ulceration over the sacrum. The results of this study indicate that there is no difference in rates of blood flow, as determined by the thermal recovery method, of skin over the sacrum and abdomen that has not been subjected to a pressure load. The higher pressure developed over the sacrum, leading to compression of blood vessels, is no doubt the major contributor to the development of pressure ulcers in this area. 70 No significant differences were found in the blood flow of skin not subjected to a pressure load when the trochanter was compared to the groin, or when the sacrum was compared to the abdomen. However, when a pressure load was applied, significant differences in the skin circulation of the susceptible and nonsusceptible areas probably exist. Areas prone to pressure ulceration such as the trochanter and sacrum, are more often exposed to high pressure than other areas, such as the groin and abdomen. In addition, the anatomy of the sacral and hip areas (thin or nonexistent layers of fat and muscle separating skin from bone) probably results in higher pressures being transmitted to the capillaries in these areas. Therefore, although there may not be a difference in skin circulation between areas prone to pressure ulceration and adjacent, nonsusceptible areas before a pressure load is applied, under conditions of pressure stress, the skin circulation of the different areas probably differs markedly. Additional Howell (1981) has reported the skin temperature values of areas prone to pressure ulceration, and of adjacent areas. Howell's findings are compared to those of the current study in Table 17. Since Howell reports only temperature ranges for the groin and abdomen, comparison of the two studies is difficult. Skin temperature values reported by Howell appear 71 to be slightly higher at all sites than the temperature observed in the current study. This may be due to measurement error, or to differences in population or environment. The general trend in both studies is similar, with the groin being warmer than the trochanter, and the sacrum and abdomen having similar temperatures. Howell explained the decreased skin temperature over the areas prone to pressure ulceration as being due to a less efficient circulation than in the adjacent areas. However, a number of factors other than skin blood flow may explain the difference in skin temperature. Skin temperature is determined by the rate of skin blood flow, the blood temperature, the thermal 72 Table 17 Baseline Skin Temperatures (0 C): Howell (n=50) and Present Study (n=30) Standard Site Mean Deviation Range Trochanter Howell Right 33.05 1.28 28.2-35.2 Left 33.22 1.45 31.0-35.2 Present Study Right 32.32 1.22 29.4-34.0 Left 33.09 1.27 31.0-36.0 -Gr-oi-n Howell Right 33.0-36.8 Left 32.4-37.8 Present Study Right 33.90 1.00 31.8-35.4 Left 33.85 1.12 31.0-35.03 Sacrum Howell 34.96 0.61 33.4-36.0 Present Study 33.30 1.22 30.5-34.9 Abdomen Howell 33.0-36.8 Present Study 33.30 1.21 30.6-35.3 Note. Adapted from Howell, 1981. 73 conductivity of the tissue, the metabolic rate, and heat loss to the environment. When measuring skin temperature in one area of the body, factors affecting skin temperature other than blood flow can be controlled. However, when comparing different areas of the body, differences in thermal conductivity and metabolic rate may contribute greatly to differences in skin temperature. The results of the current study suggest that these skin temperature fferences are not due to differences in skin blood flow, but to differences in metabo c rate of underlying tissue. Limitations Although the results of this study seem to indicate that there is no significant difference between the skin blood flow of areas prone to pressure ulceration, and adjacent, nonsusceptible areas, intervening variables may be responsible for these findings. Alternate explanations for the findings will be examined. Three unanticipated patterns emerged which may cast doubt on the validity of the thermal recovery method as performed in this study. 1. The skin temperature readings frequently continued to decrease following removal of the cold glass container. It is unlikely that this is a 74 reflection of actual skin temperature. One possible explanation for this phemonenon is that the thermistors were unable to respond rapidly enough to the relatively large changes in skin temperature. Thermistors do not directly measure the temperature of the skin. The thermometer rather displays the temperature of the thermistor, which must stabilize with the temperature of the skin if there is to be an accurate reflection of skin temperature. In this study, thermistors were placed on the areas of study, and allowed to stabilize for five minutes before baseline skin temperatures were recorded. The thermistors were then moved to just outside the ten centimeter diameter circles centered over the site. The temperature of the thermistors thus remained fairly constant up to this point. After ice was applied to the skin for one minute, the thermistors were replaced in the center of the circles, and were subjected to a large drop in temperature. The rather large thermistors used in this study (2 rnrn, diameter) may have required several measurement periods to equalize with the skin temperature. Therefore, the lowest actual skin temperature may have been lower than the lowest recorded skin temperature. This inaccuracy would affect the calculation of the PBel. Use of smaller thermistors with a more rapid 75 response time would increase the accuracy of similar studies in the future. Although the manufacturer states that the time constant of the thermistor is 1.1 seconds, and that 99% of a newly impressed temperature is read within five time constants, considerably longer than 5.5 seconds was required for temperatures to stabilize when the baseline skin temperatures were measured. The continued decrease in skin temperature following the removal of the cold stimulus may also have been due to reflex vasoconstriction. Skin vessels respond to cold by constricting (Dodd, 1979). If this constriction is marked, skin blood flow would be interrupted following the removal of cold. With little or no heat flowing into the tissue, and heat loss to the environment continuing, the skin temperature could continue to decrease. The thermoregulatory vascular reflexes are unchanged by age in healthy persons. However, there is a group of elderly who show impaired regulation of skin blood flow and are at increased risk for developing hypothermia (Hanna & MacMillan, 1976). The reflex vasoconstriction in this group could be prolonged, and the skin temperature decrease following the removal of cold would be accentuated in this group_ Some antihypertensive medications effect peripheral vascular resistance and may have accentuated 76 the skin temperature decrease. Clonidine, methyldopa, and hydralazine, taken by four subjects in this population, cause vasodilatation, and may have altered the skin's response to cold. The other antihypertensive medications taken by subjects in this study were beta blocking agents and diuretics, which probably do not have an effect on the peripheral circulation (Nickerson & Ruedy, 1975). 2. There was considerable variation between subjects in the initial decrease in skin temperature following the application of cold. The initial decrease in skin temperature ranged from 0.52° C to 8.76° C. This variation was most pronounced over the sacrum. The temperature decrease over the sacrum was significantly less than over the trochanter and abdomen, and approached significance when compared with the groin. Large variations in the initial decrease in skin temperature might result in variation in the PBCI, since large decreases in skin temperature would seem to result in slower thermal recovery, and small decreases to result in more rapid thermal recovery. However, when correlation coefficients were calculated between the initial decrease in skin 77 temperature and the PBCI, a significant correlation was noted only at the sacrum. If differences in the initial decrease in skin temperature affected the PBCI, this affect was apparent only at the sacrum. The sacrum differs from the other experimental areas in that there are no major blood vessels in the area, and there are no muscles or muscle insertions over the sacrum. These anatomical differences may have contributed to the differences in the initial decrease in temperature over the sacrum. Intervening variables which could contribute to the differences in the initial decrease in skin temperature include: a) differences in the pressures used to apply the cold glass container to the skin, which could alter the thermal conductivity at the container-skin interface, and also cause changes in blood flow; b) differences in the application or adherence of thermistors to the skin, causing a difference in the thermal conductivity at the thermistorskin interface; c) differences in the temperature of the container if the ice slurry did not cool the container to equal temperature; and d) physiologic and anatomic differences between subjects. Although the possible intervening variables were not measured, every effort was made to provide identical conditions for each subject, and no differences in the pressure used to apply cold, the application or adherence of the thermistors, or the temperature of the container were noted by the investigator. Since the variation was greatest over the sacrum, it is possible that the anatomic differences of the sacrum caused most of this variation. 78 In order to determine the validity of the thermal recovery method as performed in this study, it is recommended that the study be repeated using another method of studying skin blood flow, such as laser Doppler velocimetry. Future studies using the thermal recovery method should include measurement of the temperature of the container, and if possible, measurement of the pressure used to apply the container to the skin. Strict attention should be paid to the adherence of thermistors to the skin. 3. The differences between the mean PBels of the trochanter and groin (16 seconds) and between the mean PBels of the sacrum and abdomen (19 seconds) were less than or equal to the accuracy of the measurement as performed in this study. From a cursory examination of the difference in mean PBels, it would appear that the thermal recovery method is not sufficiently sensitive to detect small differences in 79 blood flow. However, when the absolute difference (numerical value without regard for positivity or negativity) between the PBCls of the trochanter and groin was calculated for each subject, the PBCls of the two sites were found to be identical in only two subjects, and differed by 20 seconds in only five subjects. Absolute differences in the PBCls of the groin and trochanter within each subject ranged from 0 to 220 seconds, with a mean difference of 74.7 seconds. Calculation of the absolute difference between the PBCls of the sacrum and abdomen for each subject showed only two subjects with identical PBCls at these sites. The PBCI differed by 20 seconds in only four subjects. The absolute difference in PBCI within each subject for these two sites ranged from 0 to 500 seconds, with a mean difference of 137 seconds. Although the difference of mean PBCls from site to site was small, large differences were noted on most individual subjects. The thermal recovery method appears to be adequately sensitive to detect site-tosite differences in skin blood flow. No provision was made to control the number of calories consumed by the subjects prior to participation in the study, or to measure the insulation by body fat, although these factors may influence body temperature. Since the thermal recovery method is more sensitive to variations in skin blood flow than simple measurement of skin temperature, these are probably not major limitations. 80 Small sample size may also have been a limitation in this study, contributing to type II error. Power is a statistical term used to indicate the probability of Type II error not occurring (Cohen, 1969). Assuming a difference in population means of 20 seconds, a population standard deviation of 100 seconds, and a one-tailed .05 decision rule, the power of thermal recovery method as performed in this study is about .30. In order to raise the power of the technique to .80, a sample size of 156 subjects would be required. Increasing the sample size may reveal a significant difference between the PBCls at different sites. However, considering the large variation in PBCls at individual sites, this seems unlikely. Although every attempt was made to provide similar conditions of measurement for each subject, no measurements were made of the pressure applied to the skin by the cold glass container, or of the temperature of the container. Small differences in these values may have altered the PBCls of subjects. The thermistors 81 were applied in an identical manner to each subject, but small changes in position and muscle movement may have caused displacement of the thermistor probes, resulting in erroneous values. Another source of erroneous temperature values may have been the rela-tively slow response time of the thermistors. No attempt was made to control ambient temperature or humidity. The room temperature varied only 2° C during the course of the study, and no change in room temperature was noted during the course of measurement of anyone subject, so this was probably not a major limitation. Measurements were made between one pm and four-thirty pm. Diurnal variations in body metabolism may have accounted for variations in skin temperature. No attempt was made to control for antihypertensive medications. Implications for Nursing Practice Although the validity of the thermal recovery method, as performed in this study, may be questioned, the data indicates that there is no significant difference between the skin blood flow of areas prone to pressure ulceration and adjacent, nonsusceptible areas under baseline conditions. A long-standing nursing belief is that massage of bony prominences is useful in the prevention of pressure ulcers. As usually practiced, the bony prominences are massaged after the patient has been repositioned so that pressure is no longer applied to the area, especially if the skin is reddened. The rationale for this procedure is: a) pressure ulcers are due to interruption of blood flow caused by pressure; b) reddening of the skin indicates that excessive pressure has been applied; and c) massage of the skin increases local circulation and has a protective effect. 82 Reddening of the skin indicates that vasodilatation and increased blood flow have occurred. This reactive hyperemia also occurs in other tissues. Even though no reddening of the skin may be noted, the circulation of underlying tissue may be increased following the release of pressure. It is doubtful that measures to increase blood flow would have a protective effect in this case. Massage of bony prominences to increase skin blood flow before the application of a pressure load may be more beneficial in preventing pressure ulcers. Research has shown conclusively that prolonged, excessive pressure is the primary contributor to the development of pressure ulcers, but has not shown 83 that variations in baseline skin blood flow contribute to their development. Therefore, nursing intervention should continue to concentrate on decreasing the amount and duration of pressure applied to the surface of the body. Measures to increase the local circulation are of dubious value. CHAPTER V SU~~RY AND RECOMMENDATIONS Summary Pressure ulcers are areas of localized tissue necrosis caused by prolonged, high, externally-applied pressure which limits local blood flow, resulting in anoxia and necrosis. Pressure ulcers occur most commonly in areas where high pressure develops, such as over the trochanters and sacrum. The anatomy of these areas differs from other nonsusceptible areas in that the bony prominences are covered by relatively thin layers of muscle or fat. This lack of "padding" causes higher pressures to develop in these areas. The skin vasculature is supplied by perforating arteries, which penetrate muscle and give off branches. Little information is available regarding the local skin circulation in areas prone to pressure ulceration. Decreased baseline skin blood flow could contribute to the susceptibility of these areas to pressure ulceration. 85 Little research has been conducted to determine the baseline skin blood flow in areas prone to pressure ulceration. A number of studies have examined the skin temperature of these areas. The skin temperature of unstressed areas prone to pressure ulceration was generally found to be cooler than that of other areas. Some investigators have concluded that the coolness is due to decreased skin circulation. However, skin temperature is determined by heat production of underlying tissues, thermal conductivity of the tissue, and heat loss to the environment, in addition to skin blood flow. Therefore, a more sensitive method of studying skin blood flow is required. Two studies utilizing clearance of radioactive substances to study the skin circulation of these areas were inconclusive and contradictory. The thermal recovery method is more sensitive to variations in skin blood flow than simple measurement of skin temperature. The peripheral blood circulatory index (PBCI), or the time required for the skin temperature to return half-way to normal following the application of cold, is an index of skin circulation. It has been shown to correlate well with clearance of radioactive xenon as a measure of skin circulation. The purpose of this study was to determine whether 86 there were differences in the baseline skin circulation, as measured by the thermal recovery method, between areas prone to pressure ulceration, and adjacent non-susceptible areas. The specific research questions asked were: 1. Is the PBCI over the trochanter greater than the PBCI over the groin? 2. Is the PBCI over the sacrum greater than the PBCI over the abdomen? No significant differences were found between the PBCls of any of these areas. Although a number of limitations of the study were present, the data points to a lack of difference between the skin circu-lation of susceptible and nonsusceptible areas. Nursing implications include concentrating nursing intervention on reducing magnitude and duration of pressure applied to the body, rather than on attempting to increase the local skin circulation, which is of unproven value. Recommendations for Further Research Research recommendations for further research utilizing the thermal recovery method include: 1. Using smaller thermistors with a more rapid response time. 2. Quantifying potential intervening variables such as the pressure used to apply the container of the skin and the temperature of the container. 3. Emphasizing secure attachment and adherence of thermistors to the skin. Research recommendations for further research to determine the role of local skin blood flow to the development of pressure ulcers include: 1. Repeating the study utilizing another technique of measuring skin blood flow, such as laser doppler velocimetry, to overcome the limitations of the thermal recovery method and validate the results of the study. 2. Determining quantitative changes in skin blood flow following the use of various modalities to increase skin blood flow such as massage, heat and application of topical agents. Measuring skin blood flow with the thermal recovery method or another technique before and after use of the modality. 87 3. Determining if those modalities which increase skin blood flow continue to do so after application of a pressure load. Measuring skin blood flow before and after use of the modality and after the application of the pressure load. Comparing to a control group where a pressure load is applied, but no modality to increase skin blood flow is used. 88 4. Performing animal studies to determine if increasing skin blood flow is useful in the prevention of pressure ulcers. Increasing blood flow using appropriate modality and determining the magnitude and duration of pressure required to produce an ulcer, and then comparing this to the duration and magnitude of pressure required to produce an ulcer in a control group where no modality was used. APPENDIX A INFORMED CONSENT FORM 90 I agree to serve as a subject in the investigation "Local Skin Circulation as Measured by the Thermal Recovery Method in Areas Prone to Pressure Ulceration and Adjacent Areas," conducted by Vern Hedegaard, R.N., Master of Science Candidate, University of Utah College of Nursing. The purpose of this study is to obtain information about the contribution of local blood flow to the development of pressure ulcers or bedsores. The procedures to which I will be subjected include: 1. Application of an ice filled glass container to the skin over the hips, tailbone, groin, and abdomen for one minute. 2. Measurement of skin temperature using an electrical thermometer with a stainless steel button taped to the skin at the above sites and at the opposite groin and right arm. The time required for these measurements is approximately one hour. The methods of measurement have been used before and do not involve introducing anything into the body. There may be some discomfort associated with application of the cold glass container to the skin, but no sUbstantial risks are anticipated. I understand that there may be no benefits to me personally, but that this information may lead to better methods of treating and preventing bedsores in the future. I understand that the data collected will be presented in grouped form to assure confidentiality. I am not receiving any compensation for my participation in this study. I understand that I can withdraw from this study at any time without prejudice or penalty. I have read the above and have had the opportunity to ask questions and receive answers. Signature Date APPENDIX B THERMOMETER AND THERMISTOR SPECIFICATIONS 92 Thermometer: Digitec Model: 5810 Two Ranges: -30.00 C to +50.00 C or 0.00 C to 100.00 C Resolution: 0.01 C Accuracy at 23 C + 3 C 85% r.h.: + 0.42 C for the -30.00 C to +50.00 C range; +-0.45 C for the 0.00 C to 100.00 C range Probe Inputs: Three sets on the front panel Polarity Indication: + LED indicator, displayed automatically Response Time: 500 mSec Sampling Rate: 4/sec nominal Temperature Coefficient: 0.01 C/C Operating Ambient: 0 C to 50 C Display: LED 0.4" high Power Requirements: 115/230 v AC, 50/400 Hz, 2.5 vA Battery Capacity: 7 hours typical continuous operation; 16 hours recharge from full discharge Weight: Net 2 pounds Thermistor Probes: Yellow Springs Instruments Model Number: 709A Accuracy: + 0.15 C from -30 C to 100 C Time Constant: 1.1 seconds Description: Attachable surface temperature. Stainless steel cup, epoxy backed. Easy to tape to flat surfaces. Ten foot lead attached to stainless steel cup. Time Constant: The time required for the probe to read 63% of a newly impressed temperature. Approximately five time constants are required for a probe to read 99% of the total change. APPENDIX C DATA COLLECTION SHEETS Date Time Name Subject Number Height Weight Sex Blood Pressure Medical Conditions: Diabetes Hypertension Peripheral Vascular Disease Surgical or Traumatic Scars Prior History of Pressure Ulcers Medications: Antihypertensive Medications Anticoagulants Other Trochanter to be Studied 94 Name Room Temp Pre Trochanter Pre Groin Pre Groin (Contralateral) Pre Right Brachial Pre Date Room Temp Post Time ~ V'I Name Sacrum Abdomen Right Brachial 15 I 16 17 18 20 1,,0 0"1 APPENDIX D PROTOCOL The Protocol 1. Plug thermometer into outlet, plug thermistors into thermometer. 2. Fill glass containers with ice-water slurry. 3. Approach subject in waiting area, introduce self, give brief explanation of study, and ask subject to participate. 4. Obtain subject's signature on informed consent form. 5. Weigh subject - clothed, shoes off. 6. Measure subject's height. 7. Escort subject to exam room. Have subject remove outer clothing and put on patient gown. If subject wears LDS garments, have subject remove. 8. Record room temperature. 9. Randomly select trochanter to be studied. Have subject lie on contralateral side. 10. Mark ten centimeter diameter circles over trochanter and ipsilateral groin. 11. Apply thermistor #1 to center of circle over trochanter with paper tape. 12. Apply thermistor #2 to center of circle over ipsilateral groin with paper tape. 13. Apply thermistor #3 to contralateral groin. 14. Apply thermistor #4 to right brachial region. 15. Insulate thermistors with cotton balls held in place with paper tape. 16. Allow five minutes to elapse. During this time perform steps 17 and 18. 17. Measure subject's blood pressure. 98 18. Interview subject to obtain age, medical conditions, and medications taken. 99 19. Record the initial skin temperatures from thermistors 1, 2, 3, and 4. 20. Move thermistor #1 and attach to skin just outside circle over trochanter. 21. Move thermistor #2 and attach to skin just outside circle over ipsilateral groin. 22. Gently apply ice water slurry filled containers to skin inside circles over trochanter and ipsilateral groin for one minute. Apply only enough pressure to hold the containers in place. 23. Reattach thermistors 1 and 2 to skin in centers of circles over trochanter and ipsilateral groin. 24. Record skin temperature from thermistors 1, 2, 3, and 4. 25. Continue recording skin temperatures from all four thermistors at 20 second intervals for 19 more measurement periods. 26. If, after 20 measurement periods, the skin temperature of the trochanter and groin have not returned half-way to the original skin temperature, continue recording skin temperature from all four thermistors at 20 second intervals until the temperature over the groin and trochanter has reached this point. 27. Remove thermistors I, 2, and 3 from skin. 28. Remove markings from skin with nail polish remover. 29. Mark ten centimeter circles over sacrum and abdomen. 30. Apply thermistor #1 to center of circle over sacrum. Attach with paper tape. 31. Apply thermistor #2 to center of circle over abdomen. Attach with paper tape. 32. Insulate thermistors with cotton balls held in place with paper tape. 33. Leave thermistor #4 in place over right brachial region. 100 34. Allow five minutes for stabilization of thermistors. 35. Move thermistors 1 and 2 and attach to skin just outside circles over sacrum and abdomen. 36. Apply cold glass containers to skin inside circles over sacrum and abdomen for one minute. 37. Reattach thermistors 1 and 2 to skin in center of circles over sacrum and abdomen. 38. Record ,skin temperature from thermistors 1, 2, and 4 . 39. Record skin temperature from all three thermistors at 20 second intervals. Continue recording skin temperature for 19 more measurement periods or until the skin temperature over the sacrum and abdomen has returned half-way to the initial temperature, whichever comes later. 40. Remove thermistors from skin. 41. Remove markings from skin with nail polish remover. 42. Thank subject. APPENDIX E MEAN TEMPERATURE VALUES 102 Trochanter Mean Observation Number of Temper- Standard Number Observations ature Deviation Range (0 C) 1 30 32.702 1.28 29.35-36.00 2 30 27.71 1.40 23.96-29.58 3 30 27.44 1.33 24.00-29.83 4 30 27.60 1.29 24.28-29.83 5 30 27.89 1.28 26.63-30.21 6 30 28.19 1.29 24.93-30.8 7 30 28.48 1.29 25.27-31.30 8 30 28.75 1.29 25.54-31.74 9 30 29.21 1.31 26.05-32.60 10 30 29.21 1.31 26.05-32.60 11 30 29.39 1.32 26.32-32.95 12 30 29.57 1.32 26.52-33.25 13 30 29. 75 1.33 26.78-33.53 14 30 29.90 1.35 26.94-33.82 15 30 30.06 1.36 27.12-34.05 16 30 30.20 1.36 27.32-34.27 17 30 30.33 1.37 27.49-34.46 18 30 30.45 1.38 27.62-34.63 19 30 30.56 1.38 27.71-34.79 20 29 30.62 1.38 27.82-34.91 21 28 30.74 1.40 27.93-35.03 22 16 30.31 1.23 28.05-32.57 23 12 30.39 1.35 28.18-32.64 24 11 30.27 1.20 28.29-32.30 25 10 30.17 1.06 28.33-32.10 26 8 30.08 1.15 28.35-32.17 27 7 29.85 0.86 28.39-31.10 103 Trochanter (Continued) Mean Observation Number of Temper- Standard Number Observations ature Deviation Range (0 C) 28 7 29.92 0.88 28.42-31.22 29 3 29.39 0.83 28.45-30.03 30 2 29.89 0.22 29.73-30.05 31 1 29.79 104 Groin Mean Observation Number of Temper- Standard Number Observations ature Deviation Range (0 C) 1 30 33.88 0.96 31.20-35.37 2 30 29.25 1.60 31.14-35.45 3 30 29.19 1.55 31.10-35.49 4 30 29.42 1.52 30.84-35.51 5 30 29.66 1.47 30.56-35.53 6 30 29.93 1.42 30.20-35.56 7 30 30.20 1.38 29.38-35.58 8 30 30.43 1.35 30.67-35.61 9 30 30.65 1.34 31.01-35.62 10 30 30.85 1.31 31.17-35.64 11 30 31.01 1.30 31.25-35.66 12 30 31.16 1.28 31.30-35.69 13 30 31.30 1.27 31.33-35.70 14 30 31.43 1.27 31.34-35.73 15 30 31.55 1.26 31.37-35.75 16 30 31.68 1.27 31.39-35.77 17 30 31.78 1.28 31.40-35.80 18 30 31.88 1.28 31.42-35.83 19 30 31.98 1.29 31.43-35.85 20 29 31.99 1.25 31.43-35.85 21 28 32.07 1.28 31.40-35.89 22 16 31.63 1.22 32.73-35.78 23 12 31.88 1.29 32.76-35.79 24 10 32.14 1.09 32.76-35.80 25 9 32.20 1.16 32.77-35.81 26 8 32.12 1.18 32.78-35.81 27 6 32.11 1.28 31.50-35.20 105 Groin (Continued) Mean Observation Number of Temper- Standard Number Observations ature Deviation Range (O C) 28 7 32.07 1.18 30.03-33.64 29 3 31.27 1.09 30.05-32.14 30 1 32.18 31 1 32.24 106 Contralateral Groin Mean Observation Number of Temper- Standard Number Observations ature Deviation Range (0 C) 1 30 33.87 1.15 31.20-35.37 2 30 34.04 1.14 31.14-35.45 3 30 34.04 1.14 31.10-35.49 4 30 34.04 1.17 30.84-35.51 5 30 34.05 1.21 30.56-35.53 6 30 34.05 1.25 30.20-35.56 7 30 34.03 1.35 29.38-35.58 8 30 34.08 1.22 30.67-35.61 9 30 34.10 1.19 31.01-35.62 10 30 34.11 1.18 31.17-35.64 11 30 34.12 1.18 31.25-35.61 12 30 34.13 1.18 31.30-35.69 13 30 34.14 1.18 31.33-35.70 14 30 34.15 1.18 31.34-35.73 15 30 34.15 1.18 31.37-35.74 16 30 34.16 1.18 31.39-35.77 17 30 34.17 1.19 31.40-35.80 18 30 34.17 1.18 31.42-35.83 19 30 34.17 1.19 31.43-35.85 20 29 34.13 1.19 31.43-35.85 21 28 34.13 1.22 31.40-35.89 22 16 34.14 0.94 32.73-35.78 23 12 34.18 0.97 32.76-35.79 24 11 34.26 0.97 32.76-35.80 25 8 34.20 1.02 32.77-35.81 26 8 34.05 1.05 32.78-35.81 27 7 33.51 1.19 31.50-35.20 107 Contralateral Groin (Continued) Mean Observation Number of Ternper- Standard Number Observations ature Deviation Range (0 C) 28 7 33.78 0.82 32.80-35.20 29 3 33.56 0.92 32.80-34.58 30 2 33.94 0.92 33.29-34.59 31 1 33.94 108 Right Brachial Phase I Nean Observation Number of Ternper- Standard Number Observations ature Deviation Range (0 C) 1 30 33.19 1.16 31.20-35.41 2 30 33.50 1.14 31.30-35.77 3 30 33.50 1.15 31.24-35.80 4 30 33.55 1.13 31.66-35.82 5 30 33.57 1.13 31.65-35.83 6 30 33.59 1.14 31.58-35.84 7 30 33.63 1.15 31.52-35.85 8 30 33.63 1.14 31.59-35.87 9 30 33.66 1.14 31.53-35.89 10 30 33.71 1.17 31.44-35.91 11 30 33.72 1.18 31.45-35.93 12 30 33.72 1.17 31.42-35.97 13 30 33.74 1.17 31.38-35.98 14 30 33.76 1.17 31.36-35.98 15 30 33.78 1.17 31.34-35.98 16 30 33.80 1.18 31.29-35.97 17 30 33.81 1.19 31.10-35.99 18 30 33.83 1.20 31.06-36.01 19 30 33.85 1.20 31.01-36.01 20 29 33.88 1.23 30.98-36.01 21 28 33.90 1.25 30.97-36.01 22 17 33.43 1.14 30.95-35.14 23 12 33.60 1.18 30.95-35.14 24 11 33.47 1.23 30.94-35.12 25 9 33.46 1.37 30.94-35.10 26 8 33.75 1.08 32.15-35.09 27 7 33.66 1.12 32.06-35.12 109 Right Brachial Phase I (Continued) Mean Observation Number of Temper- Standard Number Observation ature Deviation Range (0 C) 28 7 33.64 1.10 32.07-35.16 29 2 33.47 1.42 32.47-34.48 30 1 34.53 31 1 34.58 110 Sacrum Mean Observation Number of Temper- Standard Number Observation ature (0 C) Deviation Range 1 30 33.32 1.22 30.54-34.92 2 30 29.43 1. 79 25.96-32.34 3 30 29.36 1.87 25.30-32.33 4 30 29.42 1.82 25.36-32.33 5 30 29.59 1.82 25.42-32.62 6 30 28.82 1.75 25.47-32.97 7 30 29.92 1.77 25.53-33.25 8 30 30.09 1.74 25.62-33.44 9 30 30.24 1.73 25.73-33.66 10 30 30.41 1.71 25.83-33.85 11 30 30.525 1.71 25.93-34.01 12 30 30.67 1.69 26.03-34.17 13 30 30.80 1.68 26.15-34.28 14 30 30.94 1.67 26.24-34.42 15 30 31.14 1.81 26.30-34.98 16 30 31.15 1.66 26.38-34.64 17 30 31.29 1.69 26.43-34.75 18 30 31.36 1.67 26.52-34.83 19 30 31.45 1.67 26.60-34.90 20 29 31.53 1.67 26.66-34.97 21 29 31.64 1.67 26.75-35.02 22 22 31.44 1.62 26.83-34.06 23 18 31.39 1.68 26.90-34.20 24 15 31.14 1.60 26.96-33.67 25 13 31.25 1.71 27.03-33.71 26 13 31.33 1. 70 27.08-33.75 27 12 31.31 1.72 27.16-33.79 III Sacrum (Continued) Mean Observation Number of Temper- Standard Number Observation ature Deviation Range (0 C) 28 11 31.17 1.59 27.25-33.51 29 7 30.71 1.54 27.35-31.63 30 7 30.78 1.54 27.42-31.70 31 6 30.74 1.67 27.46-31.77 32 4 30.33 1.92 27.54-31.65 33 3 29.95 2.10 27.59-31.62 34 3 29.30 2.08 27.66-31.64 35 3 30.06 2.02 27.79-31.66 36 3 30.09 2.01 27.82-31.67 37 3 30.12 2.01 27.85-31.68 38 3 30.14 2.00 27.88-31.70 39 2 29.82 2.67 27.93-31.71 40 2 29.84 2.66 27.96-31.72 41 2 29.86 2.64 28.00-31.73 42 1 28.05 43 1 28.09 112 Abdomen Hean Observation Number of Temper- Standard Number Observations ature Deviation Range (0 C) 1 30 33.34 1.21 30.63-35.27 2 30 28.87 1.94 24.30-31.88 3 30 28.78 1.87 24.37-32.01 4 30 28.93 1.78 24.66-32.14 5 30 29.14 1.71 25.24-32.20 6 30 29.35 1.66 25.77-32.25 7 30 29.58 1.60 26.41-32.34 8 30 29.77 1.56 26.72-32.40 9 30 29.93 1.54 27.08-32.49 10 30 30.14 1.52 27.46-32.59 11 30 30.28 1.48 27.74-32.69 12 30 30.43 1.46 27.93-32.74 13 30 30.57 1.45 28.09-32.84 14 30 30. 70 1.44 28.31-33.26 15 30 30.80 1.43 28.47-33.40 16 30 30.93 1.43 28.55-33.78 17 29 31.14 1.39 29.13-34.01 18 29 31.23 1.39 29.22-34.12 19 29 31.32 1.39 29.28-34.25 20 29 31.39 1.40 29.31-34.36 21 29 31.50 1.38 29.36-34.42 22 22 31.215 1.17 29.38-33.38 23 18 31.27 1.22 29.42-33.46 24 17 31.28 1.21 29.48-33.53 25 13 31.31 1.29 29.51-33.60 26 13 31.27 1.27 29.61-33.68 27 12 31.25 1.19 29.64-33.73 113 Abdomen (Continued) Mean Observation Number of Temper- Standard Number Observations ature Deviation Range (0 C) 28 11 31.10 0.92 29.69-32.50 29 6 31.07 1.00 30.00-32.52 30 5 31.31 0.98 30.04-32.54 31 5 31.17 0.94 30.05-32.50 32 3 30.73 0.72 29.99-31.25 33 3 30.67 0.69 30.02-31.32 34 2 30.46 0.78 30.08-30.84 35 2 30.84 0.64 30.15-31.53 36 2 30.87 0.62 30.21-31.53 37 2 30.92 0.63 30.26-31.68 38 2 30.98 0.61 30.35-31.61 39 2 31.01 0.59 30.40-31.71 40 2 31.06 0.58 30.49-31.63 41 2 31.11 0.58 30.55-31.67 42 2 31.20 0.48 30.64-31.76 43 1 114 Right Brachial Phase Two Mean Observation Number of Ternper- Standard Number Observations ature Deviation Range (0 C) 1 30 33.87 1.12 31.09-35.29 2 30 33.73 1.24 31.22-35.04 3 30 33.73 1.25 31.14-35.07 4 30 33.74 1.25 31.13-35.01 5 30 33.77 1.27 31.10-35.07 6 30 33.78 1.27 31.10-35.07 7 30 33.79 1.27 31.09-35.06 8 30 33.80 1.28 31.07-35.05 9 30 33.76 1.26 31.03-35.08 10 30 33.70 1.27 30.97-35.10 11 30 33.67 1.28 30.94-35.13 12 30 33.69 1.29 30.92-35.15 13 30 33.74 1.29 30.94-35.18 14 30 33.78 1.24 31.22-35.19 15 30 33.80 1.18 31.27-35.21 16 30 33.81 1.16 31.25-35.23 17 29 33.77 1.14 31.25-31.15 18 29 33.77 1.13 31.26-35.17 19 29 33.78 1.11 31.25-35.19 20 29 33.79 1.11 31.25-35.21 21 29 33.81 1.10 31.23-35.22 22 21 33.56 1.12 31.23-35.23 23 18 33.63 0.98 32.21-35.23 24 17 33.65 1.01 32.23-35.23 25 13 33.92 0.96 32.29-35.24 26 13 33.92 0.95 32.35-35.24 27 12 33.91 0.99 32.31-35.23 115 Right Brachial Phase Two (Continued) Mean Observation Number of Ternper- Standard Number Observations ature Deviation Range (0 C) 28 11 34.06 0.89 32.39-32.24 29 7 34.20 0.85 33.32-35.25 30 5 34.16 1.00 33.35-35.25 31 4 34.33 1.07 33.37-35.26 32 2 34.36 1.28 33.46-35.26 33 2 34.36 1.27 33.47-35.26 34 2 34.37 1.27 33.47-35.27 35 2 34 .37 1.27 33.48-35.27 36 2 34.37 1.24 33.49-35.25 37 2 34.37 1.24 33.50-35.25 38 2 34.34 1.25 33.46-35.23 39 2 34.33 1.24 33.45-35.21 40 2 34.32 1.23 33.45-35.19 41 2 34.31 1.21 33.46-35.17 42 2 34.32 1.20 33.47-35.17 43 1 33.46 REFERENCES Argis, J. & Spira, M. 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