Dr. Levine is Clinical Associate Professor of Medicine, New York Medical College, Valhalla, NY, and Attending Physician in the Geriatrics Section, St. Vincent Catholic Medical Center, New York, NY.
This is Part I of a two-part series on pressure ulcers and Medicare reimbursement. Part II will discuss documentation of altered skin integrity and will appear in the next issue of the Journal.
 
Introduction
Medicare recently announced that as of October 2008 it will no longer reimburse hospitals and nursing homes for preventable complications; included in this list of complications are pressure ulcers.1 But who will pick up the cost, and how will Medicare determine which pressure ulcers were preventable? Healthcare facilities stand to lose millions of dollars when pressure ulcers develop in patients under their care. This situation will become more challenging for hospitals if private insurers follow the example set by Medicare. This article will review specific factors that Medicare and other insurers may consider when determining whether a pressure ulcer is preventable—a decision that will have serious financial repercussions for all organizations that provide primary care for older persons.
The new Medicare reimbursement rules reflect the surge in interest for “pay for performance,” which encourages payment only for healthcare that meets certain benchmarks of quality.2 This concept has its basis in getting value commensurate with cost, and targets measures of performance such as quality, efficiency, and patient satisfaction—which in turn translates into absence of preventable errors or complications.3 In-hospital preventable occurrences include such entities as pressure ulcers, catheter infections, transfusion with incompatible blood products, fall-related injuries, and wrong-site surgery. In the past decade, healthcare quality advocates such as the Centers for Medicare & Medicaid Services (CMS), the Joint Commission on Accreditation of Healthcare Organizations (JCAHO), the National Quality Forum (NQF), and others have endorsed the concept that pressure ulcers are directly linked to quality. Denial of payment for pressure ulcers and related complications will essentially reward institutions with low ulcer rates, providing huge incentives to prevent this complication.
The prevalence of pressure ulcers in acute care hospitals ranges from 3.0% to 15%, with most patients being elderly, and the total national cost for treatment is conservatively estimated as between $5 billion and $8.5 billion.4,5 Pressure ulcers are the most common entity on the “no-pay” complications list. In 2006, CMS found 322,946 episodes of pressure ulcers occurring as secondary diagnoses on hospital charts, which was ten times more common than the next most prevalent complication, Staphylococcus aureus sepsis.6 Costs of pressure ulcers can be measured in additional nursing time, physician visits and consultations, prolonged hospital stay, diagnostic and operative procedures, wound care products, increased need for rehabilitation services, pain and debility, and death from related complications. All experts agree that the costs of treating pressure ulcers are much greater than the costs of prevention.5
Pressure Ulcer Documentation, Prevention, and Avoidability [1 HEAD]
The presence of a timely and detailed initial skin assessment will have important implications should CMS institute a “present-on-admission” coding system. If a pressure ulcer is not documented within hours of admission, it is possible that the insurer will determine that the facility “owns” the ulcer, and the facility will risk denial of payment. Frequently, patients spend hours in the emergency room before being admitted to the medical ward or intensive care unit (ICU), and a day or two may go by before a complete nursing skin assessment is entered into the medical record. Another day or two may pass before impaired skin integrity is documented by the physician. A detailed inspection of skin condition must be conducted within hours of the patient’s arrival in the hospital or nursing home. This will mean revamping of the admission skin assessment process, with consideration of photographs to document pressure ulcers when the patient enters the facility. (Additional information on assessment and documentation will be provided in Part II.)
 Several processes of care have been identified as quality indicators related to pressure ulcer prevention, the first being daily skin assessment (Table I).7 Another component of prevention is incorporation of a risk-assessment tool such as the Braden Scale, with preventive measures put into place if a patient is scored at risk. Preventive measures may include repositioning techniques, mobilization strategies, pressure-relief devices including specialty mattresses and overlays, and timely attention to nutrition and hydration. One inter-institutional collaborative effort in New Jersey was able to reduce pressure ulcers by 70% with these low-technology interventions.8
What if a pressure ulcer is not present on admission and occurs while in the hospital? It is unclear at this time whether insurers will deny payment for all in-house–acquired ulcers, or take a more sophisticated approach by considering underlying medical conditions in determining “avoidability.” Risk stratification is essential when determining preventability of pressure ulcers, as outcome measures can only be assessed in the context of resident characteristics that contribute to the success of good medical care.9 The long-term care guidelines for surveyors offer a basis for determination of whether a pressure ulcer was avoidable:10
“Avoidable” means that the resident developed a pressure ulcer and that
the facility did not do one or more of the following: evaluate the resident’s
clinical condition and pressure ulcer risk factors; define and implement
interventions that are consistent with resident needs, resident goals, and
recognized standards of practice; monitor and evaluate the impact of the
interventions; or revise the interventions as appropriate.10
“Unavoidable” means that the resident developed a pressure ulcer even
though the facility had evaluated the resident’s clinical condition and
pressure ulcer risk factors; defined and implemented interventions that
are consistent with resident needs, goals, and recognized standards of
practice; monitored and evaluated the impact of the interventions; and
revised the approaches as appropriate.10
Although these regulations were developed for nursing homes, the same concept can apply to hospitals. When considering risk stratification related to pressure ulcer development it is important to consider the complex synergy of underlying medical conditions (Table II).
Medical Factors to Consider When Assessing Pressure Ulcer Risk [1 HEAD]
It has been noted that even in the presence of preventive measures, pressure ulcers can occur.11 Conditions that render a patient at risk for pressure ulcer development are numerous, and it is not clear which specific combination of conditions will lead to ulcer formation when prevention measures are in place. Skin failure has been recognized by some authors as an entity sometimes concurrent with severe dysfunction or failure of other organ systems.12 This section will outline potential considerations that Medicare and other insurers will look at when making the determination of preventability of pressure ulcers.
Urinary and Fecal Incontinence
It has been long recognized that the caustic effects of urine and feces have deleterious consequences for skin.13 Moisture causes maceration and can increase skin fragility and cause irritation, while introduction of coliform bacteria will increase the propensity for infection. This problem is exacerbated by hospital-acquired infections such as Clostridium difficile (C. difficile), which often results in chronic oozing of liquid stool onto the perineal area. The challenge of nursing is to keep patients clean and dry, and physicians should not forget the importance of hydration, skin assessment, and infection surveillance.
Peripheral Vascular Disease 
Patients with risk factors for peripheral vascular disease (PVD) such as diabetes mellitus, hypertension, hypercholesterolemia, and history of smoking are at increased risk for developing new ulcers of the lower extremity during hospitalization. Documentation should include assessment of these risk factors, along with physical examination of peripheral pulses and signs of trophic changes consistent with PVD. If a patient has a history of endovascular procedures or bypass of the lower extremity, this should be documented on the record. Physical examination can be supplemented by noninvasive vascular studies such as ankle-brachial index or pulse volume recordings to document the presence of PVD. In persons with advanced calcific atherosclerotic disease, ankle-brachial index can lose its specificity and can be supplemented by photoplethysmography or magnetic resonance angiogram.14 The investment in diagnostics will benefit patient management while helping to prevent claim denials from insurers looking to cut costs.
Hypotension and Hypoxia
Patients in a state of prolonged hypotension and/or hypoxia are at increased risk for developing skin ulceration due to tissue hypoperfusion, particularly in areas already under direct pressure from the body’s natural weight. Hemorrhagic shock leads directly to tissue hypoxia and hypoperfusion, while septic shock results in microvascular endothelial dysfunction causing tissue hypoxia even in the presence of adequate oxygenation.15,16 Anemia, which limits the blood’s oxygen-carrying capacity, can act synergistically in perpetuating tissue hypoperfusion, as can low cardiac output.
 From a diagnostic standpoint it is important to quantify these physiologic imbalances with appropriate examinations including vital signs, complete blood count, blood gas, and echocardiogram. Aggressiveness of medical interventions in critically ill persons should always be guided by advance directives, family wishes, and ethical considerations, all of which should be carefully documented if the record requires scrutiny by insurers to determine pressure ulcer avoidability.
Malnutrition 
Nutritional status has long been linked to pressure ulcers.17 Malnourished hospitalized patients are more likely to develop pressure ulcers, and once skin damage occurs, malnourished individuals may have impaired healing ability.18,19 In long-term care, impaired nutritional intake has been shown to be predictive of pressure ulcer development.20 It is therefore important from a clinical standpoint to get an early handle on the nutritional status of newly admitted patients. This translates into early nutritional assessment with appropriate laboratory values such as albumin and prealbumin, accurate weights, and active collaboration between nutritionist, nurse, and physician.
Hypoalbuminemia can lead to edema and anasarca due to decreased intravascular oncotic pressure. Edema can impair delivery of oxygen and nutrients to tissue, raising the risk of pressure-related injury in susceptible areas. Often considered an indicator of malnutrition, liver and kidney disease as well as protein-losing enteropathy can also interfere with albumin levels.
 A condition related to malnutrition in hospitalized patients is the catabolic, or hypermetabolic, state. This is defined as the physiologic response to a variety of stressors such as acute illness, trauma, and infection. Catabolism triggers a biomechanical cascade that results in muscle wasting, weight loss, decreased healing ability, and complex metabolic changes such as lipolysis and insulin resistance.21 The catabolic state must be recognized and addressed with aggressive nutritional management; however, it is unclear whether nutritional intervention in acutely ill older persons will forestall the occurrence of pressure ulcers.22
Diabetes Mellitus
Longstanding diabetes mellitus adversely affects both macro- and microvasculature, impairs granulocyte function, and causes neuropathy and loss of sensation. Increased glucose levels cause cell walls to become rigid, impairing blood flow through small vessels at the wound surface. This phenomenon is made worse by impaired release of oxygen by the hemoglobin molecule. White blood cells are affected by impaired chemotaxis and phagocytosis, which encourages growth of bacteria and fungus. Persons with diabetes have increased propensity to develop fungal rashes that can cause perineal irritation and skin breakdown. The presence of diabetes and hyperglycemia increases the risk for infection, which in turn can contribute to immobility and catabolic state, contributing to skin ulceration.
Gastrointestinal Disease and Malabsorption
Many gastrointestinal problems contribute to malnutrition and, therefore, increase risk for pressure ulcers. Surgical procedures such as bowel resections and fecal diversion can place patients at increased risk for poor absorption of moisture and nutrients. Other conditions such as celiac disease, Crohn’s disease, bacterial overgrowth, and gastrointestinal malignancy can cause malabsorption and micronutrient deficiencies. Chronic biliary problems such as pancreatitis and hepatitis can interfere with absorption of food with decreased bile salts and other mechanisms. Hospitalized patients with C. difficile colitis can become further compromised nutritionally and hemodynamically with severe diarrhea and development of hypoalbuminemia.23
Malignancy
Patients with cancer are at increased risk of developing pressure ulcers.24 Both gastrointestinal and nongastrointestinal malignancies can interfere adversely with nutritional status and potentially increase risk for skin breakdown. Patients with cancer can develop intestinal morphological atrophy as well as cytokine-mediated malabsorption.25 The cachexia syndrome associated with cancer is well recognized, and is characterized by weight loss, anemia, and malnutrition caused by decreased food intake.26 Although the association of tumor-related cachexia with pressure ulcer risk makes theoretical sense, there is limited research exploring the relationship between pressure ulcers and cancer.27
End-Stage Renal Disease
Because protein and energy intake decrease during the course of renal insufficiency, resulting malnutrition can lead to increased risk for pressure ulcers and decreased wound-healing ability. Inflammatory cytokines present in patients with end-stage renal disease can induce anorexia, muscle wasting, and malnutrition.28 An additional management challenge is the necessity to decrease protein intake, which can be at odds with increased protein requirements once a wound occurs.
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Case Study
Mrs. P, a 78-year-old female, was admitted to the emergency room with a fracture of her left hip after a fall at home. Her past medical history included longstanding obesity, noninsulin-dependent diabetes mellitus with microalbuminuria, diabetic nephropathy and PVD, hypertension, hypercholesterolemia, emphysema, and 40 pack-years of smoking. She had no skin ulcers on admission, and underwent open reduction and internal fixation of the hip. Postoperatively, Mrs. P developed atrial fibrillation with rapid ventricular rate and congestive heart failure, requiring intubation and transfer to the ICU, where she became hypotensive with cardiogenic shock and required pressor agents. Subsequently, she developed acute renal failure, requiring insertion of a femoral catheter for emergency hemodialysis. Nasogastric feeding was instituted, and the patient required wrist restraints because of agitation and pulling at tubing. Mrs. P developed fever and aspiration pneumonia and was administered broad-spectrum antibiotic therapy, but developed copious green diarrhea that tested positive for C. difficile enterotoxin. She was difficult to wean from the ventilator, and required tracheostomy and percutaneous gastrostomy for feeding. The patient’s right foot became dusky, and magnetic resonance angiogram showed severe aortoiliac atherosclerotic disease, with unreconstructable stenosis of the right popliteal artery. The right heel became gangrenous despite the presence of heel protectors.
 This ICU routinely employs low-air-loss beds for all patients on ventilators. On the third hospital day, Mrs. P’s sacrum was red, and by the seventh day, she had a 5-cm diameter eschar, which subsequently became infected. The physician informed the family of her very poor prognosis, but despite a living will that stated that she declined artificial nutrition and heroic life-support measures, the patient’s daughter insisted on doing “everything to keep her alive.” In the weeks following transfer from the ICU, Mrs. P underwent above-the-knee amputation of the right leg and several debridements of the sacrum, which was diagnosed with osteomyelitis. After a palliative care consult, the family finally decided to place the patient on hospice, and she died four months after the initial fall with hip injury.
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When new Medicare rules are implemented, the hospital will risk disallowance of incremental payments related to secondary conditions of sacral and heel ulcers developed during this patient’s stormy ICU stay, despite the presence of monitoring and pressure relief. However, Mrs. P had severe underlying illness including longstanding diabetes mellitus, diabetic nephropathy, emphysema, and PVD. Her ICU course was marked by prolonged hypotension with respiratory failure and hypoxemia, acute-on-chronic renal failure, and C. difficile enterocolitis with severe diarrhea. Despite a poor prognosis and advance directives prohibiting artificial life support, the patient’s family insisted on maintaining her on ventilator, pressors, hemodialysis, and tube feeding.
 It is currently not known which specific medical conditions or combination thereof will always lead to pressure ulceration. However, this patient suffered from multiple-organ-system failure and was kept alive against her wishes, developing pressure ulcers and suffering the consequences of infection, amputation, and other surgical procedures. Pressure-relief measures were in place, but repositioning was limited due to life-support measures and physical restraint that was necessary for preservation of airway access, catheters, monitors, and intravenous tubing. Although many conditions may have contributed to the unavoidability of these pressure ulcers, it is unclear how Medicare will take these and other complex ethical issues into consideration when hospital reimbursement is determined.
Conclusion
Beginning in October 2008, Medicare will no longer provide hospitals with reimbursement for conditions it deems preventable. It is likely that other insurers will follow this example. Among the preventable conditions are pressure ulcers, and hospitals stand to lose millions of dollars for this common occurrence. At present, it is unclear how insurers will decide whether an ulcer is preventable, and this question will certainly spark intense debate. Elements to consider when deciding avoidability of pressure ulcers include skin condition on admission, adequacy of skin ulcer prevention program, and presence of comorbid conditions both on admission and during the hospital stay. To meet the challenge of these reimbursement changes, hospitals must re-evaluate systems for skin assessment and wound documentation, and clinicians must increase their educational level and awareness of issues related to pressure ulcers, their prevention, and treatment.

The author owns a company that consults about wounds and wound care, and also speaks frequently on this topic.

References
1. Pear R. Medicare says it won’t cover hospital errors. The New York Times. August 19, 2007:A1.
2. Miller ME. Pay for performance in Medicare. Testimony before the US Senate Medicare Payment Advisory Commission. July 27, 2005. MedPac Website. http://www.medpac.gov. Accessed April 23, 2008.
3. Rowe JM. Pay-for-performance and accountability: Related themes in improving health care [published correction appears in Ann Intern Med 2007;146(2):151]. Ann Intern Med 2006;145(9):695-699.
4. Beckrich K, Aronovitch SA. Hospital-acquired pressure ulcers: A comparison of costs in medical vs. surgical patients. Nurs Econ 1999;17(5):263-271.
5. Pressure ulcers in adults: Prediction and prevention. Health Services/Technology Assessment Tool Website. www.ncbi.nlm.nih.gov/books/bv.fcgi?rid=hstat2.chapter.4409. Accessed April 23, 2008.
6. Rosenthal MB. Nonpayment for performance? Medicare’s new reimbursement rule. N Engl J Med 2007;357:1573-1575.
7. Bates-Jenson BM. Quality indicators for prevention and management of pressure ulcers in vulnerable elders. Ann Intern Med 2001;135:744-751.
8. Hughes JV. Group reduces number of patients with bedsores. The New York Times. August 5, 2007: B2.
9. Iezzoni LI. Risk adjustment for medical outcome studies. In: Grady ML, Schwartz HA, eds. Medical Effectiveness Research Data Methods. Rockville MD: U.S. Department of Health and Human Services; 1992:83-97.
10. Guidance to surveyors for long-term care facilities. Department of Health and Human Services (DHHA) Centers for Medicare & Medicare Services Website. www.cms.hhs.gov/transmittals/downloads/R4SOM.pdf. Accessed April 23, 2008.
11. Lyder CH, Preston J, Grady JN, et al. Quality of care for hospitalized Medicare patients at risk for pressure ulcers. Arch Intern Med 2001;161:1549-1554.
12. Langemo DK, Brown G. Skin fails too: Acute, chronic, and end-stage skin failure. Adv Skin Wound Care 2006;19:206-211.
13. Levine JM. Historical perspective: The neurotrophic theory of skin ulceration. J Am Geriatr Soc 1992;40(12):1281-1283.
14. Allen J. Photoplethysmography and its application in clinical physiological measurement. Physiol Meas 2007;28:R1-R39. Published Online: February 20, 2007.
15. Gutierrez G, Reines HD, Wulf-Gutierrez ME. Clinical review: Hemorrhagic shock. Crit Care 2004;8:373-381. Published Online: April 2, 2004.
16. Ellis CG, Jagger J, Sharpe M. The microcirculation as a functional system. Crit Care 2005;9 Suppl 4:S3-S8. Published Online: August 25, 2005.
17. Thomas DR. The role of nutrition in prevention and healing of pressure ulcers. Clin Geriatr Med 1997;13:497-511.
18. Thomas DR, Goode PS, Tarquine PH, Allman RM. Hospital-acquired pressure ulcers and risk of death. J Am Geriatr Soc 1996;44:1435-1440.
19. Thomas DR. Prevention and treatment of pressure ulcers. J Am Med Dir Assoc 2006;7:46-59.
20. Berlowitz DR, Wilking SVB. Risk factors for pressure sores. A comparison of cross-sectional and cohort-derived data. J Am Geriatr Soc 1989;37:1043-1050.
21. Saini A, Al-Shanti N, Stewart CE. Waste management - cytokines, growth factors and cachexia. Cytokine Growth Factor Rev 2006;17:475-486. Published Online: November 22, 2006.
22. Bourdel-Marchasson I, Barateau M, Rondeau V, et al. A multi-center trial of the effects of oral nutritional supplementation in critically ill older inpatients. GAGE Group. Groupe Aquitain Geriatrique d’Evaluation. Nutrition 2000;16:1-5.
23. McPherson S, Rees CJ, Ellis R et al. Intravenous immunoglobulin for the treatment of severe, refractory, and recurrent Clostridium difficile diarrhea. Dis Colon Rectum 2006;49:640-645.
24. Henoch I, Gustafsson M. Pressure ulcers in palliative care: Development of a hospice pressure ulcer risk assessment scale. Int J Palliat Nurs 2003;9:474-484.
25. Suzuki S, Goncalves CG, Meguid MM. Catabolic outcome from non-gastrointestinal malignancy-related malabsorption leading to malnutrition and weight loss. Curr Opin Clin Nutr Metab Care 2005;8:419-427.
26. Argilés JM, Busquets S, López-Soriano FJ. Cytokines as mediators and targets for cancer cachexia. Cancer Treat Res 2006;130:199-217.
27. Lyder CH. Assessing risk and preventing pressure ulcers in patients with cancer. Semin Oncol Nurs 2006;22:178-184.
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Table I
Quality Indicators for Pressure Ulcer Prevention
Risk factor assessment
Timely skin assessment
Pressure-relief strategies:
Turning and repositioning
Pressure-reducing surfaces and devices
Timely attention to nutrition and hydration
__________
Contains information from reference 7.
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Table II
Medical Factors to Consider When Assessing Pressure Ulcer Risk
Urinary and fecal incontinence
Peripheral vascular disease
Hypotension and hypoxia
Malnutrition
Hypoalbuminemia
Catabolic, or hypermetabolic, state
Diabetes mellitus
Gastrointestinal disease and malabsorption
Malignancy
End-stage renal disease
Edema or anasarca