News

The Essential Role of Oxygen in Pressure Injury Etiology

An Introduction to Pressure Injury / Ulcer Etiology and Surface Evaluation

Glenn J. Butler (1), Jody DiGiacomo (2), Scott Gorenstein (3), Edward Golembe (4), David Kenyon (5), Bok Y. Lee (6)

Life Support Technologies, Inc (1), Nassau University Medical Center (2), Winthrop University Hospital (3), Westchester Medical Center (4), Hamilton Research, Ltd. (5), New York Medical College (6)

The development and management of medical-surgical patient and support surface pressure related ischemic wounds remain one of the most confounding and costly challenges in healthcare today. For over 60 years, pressure mapping and patient comfort have been the dominant indicators for mattress selection. In 2008, CMS declined to further reimburse care-participating institutions for Hospital Acquired Pressure Ulcers (HAPU). This decision shifted pressure related wound costs back on providers and spawned the promotion of powered mattresses as the “state of the art” ulcer prevention technology.

Research Program History- The Life Support Technologies group (LSTg) provides elective and emergency wound care and hyperbaric medicine services around the New York Tri-State area and conducts about 80% of the medical/surgical hyperbaric emergencies in the region.

During hyperbaric therapy, patients must lie on hyperbaric chamber 3-inch foam monolithic mattresses that are not as pressure-relieving as powered low air loss, hospital provided bed systems. We were concerned to take inpatients off “special” powered beds and place them on a monolithic foam mat for 2 hours.

Beginning 2007, in an effort to safely provide adjunctive hyperbaric oxygen therapy to a larger population of sicker and post-surgical patients with compromised flaps/grafts and prescribed “special” hospital off-loading mattress systems, LST set out on a research mission to develop a better understand the etiology of pressure ulcers and to develop the capability of scientifically evaluating powered/non-powered pressure relieving mattress systems, beginning with stock hyperbaric mattresses.

New HAPU Terminology- Our research team view pressure related injury as a multi-step process that we designated as Pressure Acquired Ischemic Injury/Ulcer. The National Pressure Ulcer Advisory Panel (NPUAP) has defined this delineation as Hospital Acquired Pressure Injury*. We recognize the new NPUAP terminology and have coined the term “Hospital Acquired Pressure Injury / Ulcer (HAPI/U) in order to help standardize terminologies with the NPUAP that we use in our research and publications.

(* THE National Pressure Ulcer Advisory Board has ELECTED TO UTILIZE THE TERM “INJURY” RATHER THAT “ULCER” TO DESCRIBE THE initial POST ISCHEMIC INJURY PHASE THAT MAY LEAD TO AN ULCER.)

New Mattress Evaluation Technology- Our research technology permits real-time, simultaneous analysis of patient/mattress interface pressures and deep tissue blood perfusion as measured by NDIR Spectrographic Oxyhemoglobin interrogation. Other real-time spectrographic analyses are under development.

Our manned research outcomes demonstrate that mattress/patient interface pressure and relative blood/oxygen perfusion do not inversely correlate, and pressure is not a meaningful, real-time indicator of tissue ischemia and risk of pressure ulcer development.

Developed in our research is a real-time sensor system to simultaneously measure and record these parameters over the anatomical sites at risk for development of wounds. Measurements focused heel, sacrum, trochanter, ischium, scapula and occipital areas. A modified pressure mapping system is used for interface pressure measurements and integrated with multiple Near IR sensors to measure specific deep tissue hemoglobin Saturated Oxygen or SO2.

Traditional Pressure Mapping- LST first turned to the industry standard of mattress “pressure mapping” systems on the market today. Several systems are commercially available, and this basic technology has been used to design and promote all the commercially available clinical and retail mattress systems on the market today.

Over the last 60+ years, dozens of clinical mattress designs have been produced to help better distribute, or periodically reduce, pressure on anatomical areas of the body at higher risk for the development of pressure ulcers. All of the scientific data that has been developed to support mattress manufacturers’ claims have been based on patient/mattress interface pressure (mmHg) measurements.

Our research demonstrates that available commercial pressure mapping contains variables that make them singularly unreliable for evaluating or comparing pressure off-loading. In figure 1, we have the same 240 lb. male on the same mattress and using the same mapping system. In a space of 30 seconds, we adjusted the electronic gain up 200 percent with the noted dramatic changes in recorded interface pressure. This represents an unacceptable opportunity for data manipulation and experimental error. 1

Figure-1

Most of us have been taught that approximately 30mm Hg tissue pressures will result in capillary vessel collapse and a reduction of blood flow leading to ischemia. Yet we often see much higher interface pressures in basically healthy individuals without developing any pressure injury while many compromised patients with co morbidities begin to have ischemic changes almost immediately despite our best efforts to off-load the patient. There is clearly a lot more going on than we understand.

Deep Tissue Oxygen Tensions- we soon realized that measuring patient/mattress interfacial pressures alone were not a meaningful predictor of tissue ischemia/reperfusion (I/R) injury leading to a pressure injury and ulcers. In fact, deep tissue blood perfusion as measured by oxygen tensions seem to be the only reliable “real-time” indicator of relative tissue ischemia leading to a true reperfusion injury and pressure ulcer development.

Clearly, pressure is only one of several contributors to the pathophysiology and relative risk of pressure injury/ulcer development. Factors such as blood perfusion, BMI, nutrition, and co-morbidities affecting Nitric Oxide (NO) auto-regulation/vasodilatation and the physiological management of reactive oxygen species (ROS) all play an important part in relative pressure ulcer risk.

Can Age and Co-Morbidities Effect Risk?- Our research is demonstrating that young and healthy individuals are better able to sustain higher tissue pressures longer and still demonstrate normal active hyperemic response and blood oxygen tensions above the ischemic threshold of 40mmHg.

Conversely, older patients with co­morbidities that can compromise autoregulation appear to lose tissue oxygen tensions faster under moderate pressure (50mmHg) and do not demonstrate a normal active hyperemic response, and tend to maintain lower pressure tissue oxygen levels than starting tensions. More research is underway to evaluate this trend. Low Nitric Oxide values/response are most suspect.

Pathophysiology of Pressure Injury and Ulcer Development

It is widely accepted that the prime causal factor for the development of pressure ulcer and subsequent ulcers consists of excessive tissue pressure loading sustained for time periods sufficient to cause pressure prone tissue to become ischemic, then hypoxic, leading to reperfusion injury, ulcer and necrosis.

Since nearly all inpatients are in bed for eight hours or more, the mattress system selected for clinical use becomes a significant variable in the reduction and/or relief of pressure on the patient’s body, particularly over bony prominences. Any increase in mechanical stress (pressure and shear) further affects the availability of nutrients, such as oxygen, to susceptible tissues.

Ischemia leading to hypoxia is the result of decreased blood flow to the cutaneous tissue after prolonged periods of elevated tissue interface pressure. The resulting reperfusion injury causes neutrophil capillary endothelium adherence, cell rolling, sludging, and clotting that inhibits/occludes blood nutrient and oxygen supply.

2

Figure-2

The Ischemia–Reperfusion Injury Cycle (Fig. 2) Pressure or occlusion decreases blood flow and increasing hypoxia then forces tissue cells to use anaerobic pathways to produce ATP energy and causes more lactic acid to accumulate, resulting in greater acidosis, as well as increased quantities of hydrogen ions and more potassium around the cell.In normal individuals, this biochemical cascade of metabolites and oxygen radicals should lead to nitric oxide (NO) release and up-regulate other vessel vasodilators (active hyperemia)that promote increased fresh blood flow with oxygen and nutrients to the tissues.

The Pressure/Oxygen Relationship- The generally accepted hypothesis is that there is a close correlation between an increase in tissue pressure and a reduction in blood flow, with approximately 30mmHg pressure, resulting in capillary vessel collapse. In fact, our testing demonstrated that an increase in tissue pressure and that tissue’s blood flow as measured by oxygen saturation did not necessarily inversely correlate. Meaning that high interface pressure often did not mean a lower tissue-oxygen saturation values leading to ischemia and that a lower tissue interface pressure did not always result in better blood flow and higher oxygen saturation.

Our research also demonstrated that an increased tissue-oxygen phenomenon is only demonstrated when subjects were lying on equalized weight redistribution surfaces that provide for maximum immersion, enveloping all bony prominences in a three-dimensional format (length, width, depth) that conforms to the anthropometric characteristics of the human body.

This oxygen phenomenon is not demonstrated in equalized weight redistribution surfaces (low air loss and alternating pressure), which accommodate the human body in a two-dimensional format that forces the body to ride on top of the inflated cells without means to envelop bony prominences. This method of periodically delivering high/low pressure over a small area of the body (the width of some air cells in alternating pressure mattresses) can lead to a reduction in subcutaneous tissue oxygen saturation. In fact, it is possible to induce reactive hyperemia and resulting pressure injury with an improperly adjusted pressure alternating mattress system.

Simultaneous Pressure and Oxygen Measurements — A Complete Picture

Simultaneous measurement of both pressure and deep tissue oxygen tensions provide a more complete picture of the effects of pressure and any blood flow reduction resulting in lower oxygen tensions leading to ischemia. To solve this problem, we modified and integrated near infrared spectrographic oximetry used to measure brain oxygen during anesthesia (tissue oxygen saturation) into our existing pressure-mapping system, as a further indicator of blood perfusion and a direct indicator of tissue oxygen tension. The combination of simultaneous pressure and oxygen tension has permitted us to truly evaluate off-loading system designs and to better evaluate patients well beyond the accepted methods of a relative risk of pressure ulcer development alone.

Weight Redistribution Analysis

Figure 3 is an example of pressure-only weight distribution map on the same subject and mattress system lying down and then sitting with the bed raised to a 45-degree position.

3

Figure-3

These two pressure maps depict the weight transfer from the torso in the supine (laying down) position and weight transfer down to the sacrum and ischium anatomical areas when in a 45-degree sitting position. With many bedded and wheelchair patients spending a majority of time in a sitting or upright position, the sacrum, ischium, and heels are a primary concern.

But what is actually happening to the blood perfusion and/or any ischemic changes taking place in these at-risk tissues? Further, is there any difference in blood perfusion values and pressure injury risk between a 45-year old brittle diabetic motorcycle rider (smoker) with a broken hip and a healthy 86-year old who slipped on ice and broke a hip. The fact is the 45-year old is at significantly greater risk.

Real-time Simultaneous Pressure/Oxygen Measurements- An example of our simultaneous interface pressure/tissue oxygen analysis is depicted in Figure 4. For clarity in this graph, we are looking at only ischium pressure and oxygen values. Our standard studies simultaneously include scapula, ischium, sacrum, trochanter, and heels.

4

Figure-4

In figure 4, the subject goes from a standing position to supine for a 20 minute period, then is elevated to a 70-degree reclining position for an additional 20 minutes and then, finally, returns to a standing position.

Note that in both standing and supine positions, ischial tissue oxygen saturation averaged 55% while ischium pressure averages 26mmHg in the supine position. In the 70-degree position, the subject’s weight transfers to the ischium and the average interface pressure rises to 99mmHg while the ischial oxygen tension only decreases to 51%.

The net pressure increase from the supine to sitting is over 280%, but the oxygen only decreases by 6.5% from the supine position. This is an effect of the human body’s ability to autoregulate blood perfusion as measured by oxygen saturation.

This is a typical example of how pressure and blood perfusion are not inversely proportional in healthy subjects able to carry out normal autoregulation/active hyperemia.

Conversely, it helps us better understand how age and co-morbidities compromise blood perfusion auto-regulation, hyperemia, I/R, and pressure ulcer development.

Active Hyperemia- Active hyperemia is a normal physiological process that automatically compensates for reductions in blood flow due to transient vessel occlusions or increased tissue-interface pressures, such as prolonged sitting in healthy persons. (Fig.4) As we sit, autonomic receptors sense that our gluteus muscles are becoming ischemic and congested with metabolic byproducts. We unconsciously shift our weight to allow normal active hyperemia to vasodilate the muscles and flush the tissues with fresh blood. We can repeat this amazing process hundreds of times a day without long term effect.

As persons become older, develop co-morbidities such as diabetes, associated neuropathy, paraplegia, or compromised mentation, they become less able to initiate normal autonomic active hyperemia vasodilatation and become more susceptible to pressure-related ischemia leading to hypoxia, reperfusion injury, and necrosis.

During active hyperemia, blood flow increases because the increased oxygen consumption during muscle contraction up-regulates the production of vasoactive substances that dilate the blood vessels. Some other examples include the increase in gastrointestinal blood flow during digestion of food, the increase in coronary blood flow when heart rate is increased, and the increase in cerebral blood flow associated with increased neuronal activity in the brain.

Active hyperemia is due to a complex biochemical reaction to a combination of transient hypoxia and the generation of cell metabolites vasodilation up-regulators such as potassium ion, carbon dioxide, adenosine, and nitric oxide.

Reactive Hyperemia- Reactive hyperemia occurs after the normal physiological mechanisms of active hyperemia are exhausted. It is the next step in the biochemical cascade towards reperfusion injury. The only meaningful variables seem to be patient co-morbidities that downregulate autonomic vasodilation and tissue oxygen tension recovery times that allow tissues to become ischemic long enough to induce a true reperfusion injury.

Reactive hyperemia is the transient uncontrolled increase in blood flow that occurs following some prolonged period of ischemia. Reactive hyperemia can follow the removal of a tourniquet, unclamping of an artery during surgery, or restoring flow to a coronary artery after reopening a closed artery using an angioplasty balloon or clot dissolving drug. It also can occur after a prolonged period of tissue pressure that reduces blood flow in prone anatomical locations such as the sacrum, ischium, trochanter, scapula, thoracic spine, and heels.

When Repetitive Reactive Hyperemia Leads to Ischemia-  If the patient’s position is changed often enough, (classical two-hour nursing turn)or after a mild ischemic incident, some focal tissue pressure will be released and there will be some moderate active hyperemia and blood vessel dilation. This increases blood flow and flushes out metabolites/free radicals and then a normal blood flow autoregulation will resume. This is a normal process.

Excessive and repetitive ischemia, hypoxia, and then repetitive reactive hyperemia will lead to a true ischemia/reperfusion injury and neutrophil adherence to the capillary endothelium that then results in cell rolling, sludging, and progressive blood flow reduction/occlusion.

This repeated ischemia/reperfusion injured tissue becomes increasingly compromised and susceptible to pressure ulcer development upon repeating this vicious cycle.

For patients with co-morbidities and more prone to pressure ulcer development, the anatomical areas most susceptible to pressure and shear are the scapula, the sacrum, the ischium, trochanter, and heel. For seated and wheelchair patients, the areas most impacted are the buttocks and the ischium.

The role of shear forces developed in sitting with respect to tissue trauma in the region of the ischial tuberosities may be significant in pressure ulcer causation. Prior study results have shown that cutaneous pulsatile flow measured at the buttocks of the geriatric hospitalized patient and seated paraplegics is considerably reduced compared with that of healthy subjects.

Average skin shear values developed by a geriatric hospitalized group were three times that of a young, healthy group. It also has been shown that the sitting shear force developed by paraplegics is considerably greater than corresponding measurements of normal subjects. We think this is due in part to neuropathy affecting muscle tone and normal active hyperemia vasodilation.

Reactive Hyperemia Clinically Demonstrated- Using our simultaneous Near-Infrared Spectrographic Tissue Oximetry/Interface Pressure system we have noted that about 80% of normal test subjects demonstrated some reactive hyperemia (RH) of the sacrum; in particular, upon standing after being supine on a mattress surface for a 90-minute test period. This is the first time this has been demonstrated.

As an extreme example of this phenomenon, the Life Support Technologies (LST) lab group tested a standard three-inch memory foam mattress designed for use in monoplace hyperbaric chambers. This testing was initiated because of LST clinical concerns regarding this mattress’ ability to adequately off-load compromised patients receiving hyperbaric oxygen therapy over a two-hour supine period.

5

The degree of reactive hyperemia was sometimes significant. As an example, Subject # 4 went from a pre-test sacral area oxygen saturation value of 76%, then down to a value of 45% over a 90-minute period while supine and as immobile as possible to simulate a paraplegic/insensate patient. Most subjects experienced ever increasing to eventual extreme pain in the sacral area during this 90-minute supine/immobile test period.

Upon standing, the subject’s sacrum oxygen levels went immediately up to over 95% oxygen saturation (instrument full scale) and remained in that fulminant reactive hyperemic level for a 13 minute period before normalizing (autoregulation) back to 65–68% (Note: below test start baseline). On standing, the subject noted an extreme sensation of heat and interruption of pain.

A paraplegic subject’s sacrum became so ischemic we had to interrupt the test after only a 30 minute period. We again attribute this to neuropathy affecting muscle tone and normal active hyperemia vasodilation. This subject had no pain sensation.

This further demonstrates that neurologically compromised and para- quadriplegic patients are physiologically largely incapable of functional active hyperemia well beyond any sensation of ischemic pain.

We consider the magnitude of this reactive hyperemia as a hallmark of a true “reperfusion injury” and an early indicator of pressure injury and ulcer development.

Repetitive Ischemia/Reperfusion Injury Syndrome- We theorize that significant and repetitive changes in oxygen tensions that induce a reactive hyperemia will likely — over time — result in a repetitive ischemic/reperfusion injury syndrome that forces tissues into anaerobic cell respiration pathways, pressure injury and eventual necrosis. Figure 6 represents a theoretical progression of I/R over patient turning cycles.

6

Figure 6

The three peaks on the right side of the graph are extrapolated from actual test results depicted in the two graph peaks at the left side of the graph. These two events (the first peak is from Fig. 5) were 90 minutes apart with a 13- minute and then a 17-minute uncontrolled reactive hyperemia of the subject’s sacrum.

Based on our other test results to date, we believe that this extrapolated data is representative of the actual progression of repetitive ischemia and hypoxia is leading to significant I/R injury and neutrophil adherence to the capillary endothelium that results in cell rolling, sludging, and a progressive blood flow reduction/occlusion. The authors are presently developing a murine animal model in order to further demonstrate and research this phenomenon.

Conclusions from this research

1- The preponderance of the literature and our research supports our conclusion that pressure alone has demonstrated not to be a reliable real-time indicator of mattress design superiority or to measurably reduce pressure injury risk or ulcer incidence.

2- The pathophysiology of pressure ulcer development is just beginning to be understood. The true dynamics of repetitive ischemia/reperfusion injury as they relate to deep-tissue oxygen/nutrient supply and cell metabolite management are critical to pressure injury prevention, ulcer development, and wound care.

3-Reactive hyperemia must be avoided. The time and tissue interface pressures required to induce an ischemic/reperfusion (I/R) event vary significantly from patient-to-patient with age, co-morbidities, and functional circulatory auto-regulation.

4- Repetitive I/R injury syndrome data supports the hypothesis that repetitive reactive hyperemia inducing I/R produces ever-increasing neutrophil adherence to capillary endothelium that progressively reduces tissue-perfusion and tissue-oxygen tensions. This time and pressure is very variable and requires additional study.

5- Repetitive ischemia/reperfusion injury syndrome is a term the authors developed to describe the cyclic changes in blood flow in an immobile patient’s tissue contact area under repeated pressure and off-loading cycles when a patient is periodically turned. This phenomenon can also be induced by a misadjusted alternating mattress.

6- Medical institutions are being sold an ever-growing array of increasingly complicated and costly powered mattress systems ostensibly developed to further reduce pressure injury ulcer risks with each new design. New mattress designs are still based on interface pressure mapping and have not been able to produce measurable improvements in patients’ deep-tissue, oxygen-saturation levels, or improved patient comfort, or reduced insomnia.

7- All types of mattress systems must be designed to either permit patients to induce normal active hyperemia by patient movement or to simulate movement in an insensate/non-moving patient to induce normal active hyperemia for them. 8- Powered mattress systems were compared with the Oxy-Mat™ in independent clinical trials. Oxy-Mat™ has been credited with improved patient sleep, some reduction in pain medication, and the improved ability to participate in P/T rehabilitation.

8- It is estimated that 90%+ of hospital and long-term care facility patients are capable of normal active hyperemia and should be placed on non-powered equalizing mattress systems. The over-utilization of powered mattress systems likely represents a significate unnecessary cost in health care and may be a contributing factor in clinical outcomes and longer length of stay. In addition, clinical observations seem to support the role of sleep deprivation as a causative factor in increased length of stay.

The published research paper relating to this subject is available:

A PubMed Abstract is available here

Published paper detailing the development of the OXY-MAT™:

Butler G, Kenyon D, Golembe E, et al. Oxy-Mat Mattress System Development Utilizing Simultaneous Measurement of Interface Pressure and Deep Tissue Oxygen Saturation. Surg Tech Int. 2015;XXVI:71-82.

Click here to ORDER a PDF of the full paper

 

References

  1. Lyder CH, Wang Y, Metersky M, et al. Hospital-acquired pressure ulcers: results from the national Medicare Patient Safety Monitoring System study. J Am Geriatric Soc 2012 Sep;60(9):1603–8.
  2. Rithalia S. Assessment of patient support surfaces: principle, practice and limitations. J Med Eng&Tech. 2005;29(4):163–9.
  3. EHOB, Inc. Support Surface Principles Based on Scientific Fact. http://www.ehob.com http://www .ehob .com/pdf/support surface principles .pdf. Accessed June 11, 2014.
  4. Mcinnes E, Jammali-Blasi A, Cullum N, et al. Support surfaces for treating pressure injury: a Cochrane systematic review. Int J Nurs Stud 2013;50(3):419–30.
  5. Geyer MJ, Brienza OM, Karg P, et al. A randomized control trial to evaluate pressure-reducing seat cushions for elderly wheelchair users. Adv Skin Wound Care 2001;14(3):120–32.
  6. Black J, Berke C, Urzendowski G. Pressure ulcer incidence and progression in critically ill subjects: influence of low air loss mattress versus a powered air pressure redistribution mattress. J Wound Ostomy Continence Nurs 2012;39(3):267–73.
  7. Zamboni WA, Roth AC, Russell RC, et al. Morphologic Analysis of the Microcirculation During Reperfusion of Iscemic Skeletal Muscle and the Effect of Hyperbaric Oxygen. Plast Reconstr Surg 1993;91(6):1110–23.
  8. Zamboni WA, Stephenson LL, Roth AC, et al. Ischemia-reperfusion injury in skeletal musc;e: CD 18-dependant neutrophil-endothelial adhesion and arteriolar vasoconstriction. Plast Reconstr Surg 1997;99(7):2002–7.
  9. LaVan FB, Hunt TK. Oxygen and wound healing. Clin Plast Surg 1990;17(3):463–72.
  10. Jonsson K, Hunt TK, Mathes SJ. Oxygen as an isolated variable influences resistance to infection. Ann Surg 1988;208(6):783–7.
  11. Russo CA, Seiner C, Spector W. Hospitalizations Related to Pressure Ulcers, 2006. Rockville, MD: Agency for Healthcare Research and Quality, US Dept. of Health and Human Services; December 2008. HCUP Statistical Brief #64.
  12. Berlowitz D, VanDeusen Lukas C, Parker V, et al. Preventing Pressure Ulcers in Hospital: A toolkit for Improving Quality of Care. Rockville, MD: Agency for Healthcare Research and Quality, US Dept of Health and Human Services; April 2011. Publication #11-0053.EF.
  13. Jarrett NM, Holt S, LaBresh KA, et al. Evidence-Based Guidelines for Selected, Candidate, and Previously Considered Hospital-Acquired Conditions: Final Report. https://www.cms.gov/Medicare/Medicare-Fee-for-Service-Payment / HospitalAcq Cond/Downloads/Evidence-Based-Guidelines. pdf. Published May 1, 2013. Accessed May 13, 2014.
  14. Defloor T, Grypdonck MF. Pressure ulcers: validation of two risk assessment scales. J Clin Nurs 2005;14(3):373–82.
  15. Bader D, Oomens C. Recent Advances in Pressure Ulcer Research. In: Romanelli M, Clark M, Cherry GW, Colin D, Defloor T, eds. Science and Practice of Pressure Ulcer Management. Springer 2006:11–26.
  16. Peirce SM, Skalak TC, Rodeheaver GT. Ischemia-reperfusion injury in chonic pressure ulcer formation: a skin model in the rat. Wound Repair Regen 2000;8(1):68–76.
  17. Tsuji S, lchioka S, Sekiya N, et al. Analysis of ischemia-reperfusion injury in a microcirculatory model of pressure ulcers. Wound Repair Regen 2005;13(2):209–15 .
  18. Katori M, Anselmo OM, Busuttil RW, et al. A novel strategy against ischemia and reperfusion injury: cytoprotection with heme oxygenase system. TransjJI lmmunol 2002;9(2-4):227–33.
  19. Wang WZ, Anderson G, Fleming JT, et al. Lack of nitric oxide contributes to vasospasm during ischemia/reperfusion injury. Plast Reconstr Surg 1997;99(4):1099–1108.
  20. Colin D, Loyant R, Abraham P, et al. Changes in sacral transcutaneous oxygen tension in the evaluation of different mattresses in the prevention of pressure ulcers. Adv Wound Care 1996;9(1):25–8.
  21. Cullum N, Deeks J, Sheldon TA, et al. Beds mattresses and cushions for pressure sore prevention and treatment. Nurs Times 2001;97(19):41.
  22. Woods, Susan (2010). Cardiac Nursing. New York: Lippincotts. p. 955.
  23. Freeman, Neil S, Kotzer N, Schwab RJ. Patient Perception of Sleep Quality and Etiology of Sleep Disruption in the Intensive Care Unit. Am J Respir Crit Care Med 1999 159;(4):1155–62.
  24. Bihari S, McEvoy R, Matheson D, et al. Factors Affecting Sleep Quality of Patients in Intensive Care Unit, JCSM 2012;8(3):301–7.
  25. Proske U, Gandevia SC. The Proprioceptive Senses: Their Roles in Signaling Body Shape, Body Position and Movement, and Muscle Force. APS Physiological Reviews 2012;92(4):1651–97.

Roll R, Gilhodes JC, Roll JP, et al. Proprioceptive Information Processing in Weightlessness.

LifeSupport-USA.com

Post Comment

Your email address will not be published. Required fields are marked *