Nutrition plays an important role in the prevention and treatment of pressure injuries (PIs). Macro- and micronutrients are required by each organ system in specific amounts to promote growth, development, maintenance, and repair of body tissues. The 2019 European Pressure Ulcer Advisory Panel (EPUAP), National Pressure Injury Advisory Panel (NPIAP), and Pan Pacific Pressure Injury Alliance (PPPIA) Prevention and Treatment of Pressure Ulcers/Injuries: Clinical Practice Guideline (EPUAP/NPIAP/PPPIA CPG) provides guidance on the prevention and management of PIs.1 This guideline was a collaboration between the EPUAP, NPIAP, and PPPIA with the assistance of 14 associate organizations. The goal of this international collaboration was to provide an updated, comprehensive review of the research literature and develop recommendations reflecting recent evidence. The intent is for health professionals around the world to use the recommendations generated to prevent and treat PI.
The purpose of this article is to review the nutrition-related recommendations presented in the EPUAP/NPIAP/PPPIA CPG, and to discuss nutrition for PI management in the context of the recommendations. The recommendations were developed using a rigorous methodology outlined in the guideline in print and online (internationalguideline.com). Each recommendation includes a list of implementation considerations. Table 1 presents the nutrition-related recommendations from the EPUAP/NPIAP/PPPIA CPG, including the strengths of evidence and assigned recommendations. With the recommendations presented in Table 1 in mind, this article will discuss the underpinning research and the context in which the recommendations are implemented in the nutritional management of individuals with or at risk of PIs.
NUTRITION AS A RISK FACTOR FOR PRESSURE INJURIES
A large body of prognostic research has reported on the influence of impaired nutrition on the risk of PI in adults. As reported in the EPUAP/NPIAP/PPPIA CPG, of 50 prognostic studies reporting multivariable analyses that included at least one measure of nutrition status, 40% identified a measure of nutrition as a significant predictor of PIs. This suggests there is a moderate statistical association between nutrition status and developing a PI. The EPUAP/NPIAP/PPPIA CPG recommends providers consider the impact of impaired nutrition status on the risk of PI (Table 1).1 Impaired nutrition has not been included in pediatric PI risk factor studies to date; however, it is reasonable to assume that this guideline recommendation is also relevant to neonates and children.
The research on PI risk factors reports a wide selection of measures that can be used to identify impaired nutrition, including food intake, a medical diagnosis of malnutrition, skin fold thickness, arm circumference, weight, body mass index (BMI), nutrition assessment scales, and so on. Some of these measures are included in nutrition screening tools and have been validated as predictors of impaired nutrition.2–4 However, there is low consistency regarding the significance of these outcome measures as positive predictors for PI. For example, “food intake” was reported as significant in only 46.7% of studies that included that measure in a multivariate analysis.5–19 There are numerous contextual considerations and limitations to this prognostic research. The variability in research quality, choice of other outcomes, and the number of participants all influence the results. Few studies had an adequate number of participants with extremely low or high weights/BMIs in the sample.
Translating research into clinical practice requires clinical judgment informed by knowledge of the literature.1 When undertaking a PI risk assessment, the use of clinical judgment that considers the individual’s overall presentation and the significance of that individual’s nutrition status is required. For example, if an individual presents with other risk factors considered highly predictive of PI risk (eg, immobility), and the individual’s clinical condition is vulnerable, nutrition should be considered when assessing that individual’s PI risk.1,20,21
Nutrition status is included on most of the commonly used PI risk assessment tools, including those for specific populations such as pediatric or critically ill patients.20,22–26 In prognostic studies, nutrition assessment scales were not significantly predictive of PIs. Only one of 16 (6.3%) reported a nutrition assessment scale as a significant factor in a multivariate analysis.18 In that study, data from 170 participants recruited prospectively in a private hospital were analyzed. From 16 factors included in the predictive model, five were statistically significant, including scores on the Subjective Global Nutrition Assessment (P < .001).18 However, when used as a part of an overall structured PI risk assessment in conjunction with clinical judgment, findings from a PI risk scale can guide nutrition (and other) care planning.
Malnutrition involves several disorders that include undernutrition, obesity, and abnormal micronutrient levels. Other nutrition-related disorders that impact an individual’s nutrition status include frailty, sarcopenia, and cachexia, which have multifaceted pathogenic origins.27 The European Society for Parenteral and Enteral Nutrition (ESPEN) defines malnutrition as “a state resulting from lack of intake or uptake of nutrition that leads to altered body composition (decreased fat free mass) and body cell mass leading to diminished physical and mental function and impaired clinical outcome from disease.”27,28
Several organizations have defined criteria to diagnose malnutrition. Most recently, the Global Leadership Initiative on Malnutrition developed criteria to help identify malnutrition in adults in healthcare settings, consisting of three phenotype characteristics (weight loss, low BMI, decreased muscle mass) and two etiologic characteristics (decreased food intake or assimilation and disease burden/inflammation). The presence of one phenotype and one etiologic characteristic is required.29Table 2 outlines the malnutrition criteria used by different organizations.
Malnutrition and PIs
Meeting the body’s nutrition requirements is essential to promote health and well-being. Although the point at which inadequate nutrient intake affects skin integrity has not been defined, it is known that decreased acceptance of food and fluids/water and weight loss are associated with PIs. Also, insufficient nutrient intake and low body weight are both associated with impaired wound healing.5,30–35
International research suggests there is a relationship between nutrition and PI prevalence. In the US, a study of 2,425 patients concluded that 76% of participants were malnourished.36 An Australian study conducted in acute and long-term care settings found that, for adults with malnutrition, the odds ratio of developing a PI was 2.6 (95% confidence interval [CI], 1.8-3.5) in acute care settings, and 2.0 (95% CI, 1.5-2.7) in long-term care.37 In Japan, a study by Iizaka et al32 examined the impact of nutrition on the development and severity of PIs in home care. The sample consisted of 290 patients with PIs and 456 patients without. Researchers reported the prevalence of malnutrition was higher in older adults with a PI.32 Similarly, a Belgian study found that the odds ratio of an older adult with a PI being malnourished was 5.02 (95% CI, 1.69-14.92; P < .01).33
Malnutrition is a major health concern in community-dwelling older adults. A meta-analysis analyzing data from 111 studies conducted in 38 countries (n = 69,702) reported that malnutrition ranges from 0.8% in Northern Europe to 24.6% in Southeast Asia. In this systematic review, older adults receiving home care had the highest prevalence of malnutrition (14.6%). It was also more prevalent in rural versus urban communities (9.9% and 5.7%, respectively).38
Decreased intake of calories, protein, vitamins, and minerals is commonly seen in individuals with malnutrition, which is often associated with undernutrition. This results in unplanned and undesired weight loss, protein-calorie malnutrition, decreased BMI, reduced muscle mass, and dehydration, all of which are linked to PIs.39,40 Unplanned or involuntary weight loss is considered a major risk factor for both malnutrition and PI development.41
Overnutrition is a form of malnutrition in which the amount of nutrients consumed exceeds the amount of nutrients needed to support growth, development, and metabolism. Overnutrition can result in individuals becoming overweight and obese. In 2013, the American Medical Association acknowledged obesity as a disease that should be medically treated.42
In the US, the rate of obesity has reached epidemic proportions. The CDC reported its prevalence was 39.8% in 2015 and 2016.43 Obesity has been linked to health conditions such as cardiovascular disease, diabetes, cancer, hypertension, dyslipidemia, respiratory problems, and impaired wound healing.43
Comorbidities such as skin infection, dehiscence, PIs, and venous ulcers are common in obese individuals. These conditions occur because of hypoperfusion and ischemia in subcutaneous adipose tissue. Hypovascularity also contributes to the prevalence of PIs in patients who are obese.44 The decreased mobility and difficulty with self-repositioning often associated with individuals who are obese or extremely obese further increase the risk of PI development. Microorganisms that are attracted to the moist environment created by skin folds contribute to infections and tissue injuries.44
This is defined as “the process of identifying patients, clients, or groups who may have a nutrition diagnosis and benefit from nutrition assessment and intervention by a registered dietitian nutritionist.”45 Recognizing that nutrition screening helps to identify and treat malnutrition in patients with or at risk for a PI, the EPUAP/NPUAP/PPPIA CPG recommends it for all individuals at risk of a PI (Table 1). Any member of the interdisciplinary team who has been educated on screening tools can use them, and screening can be conducted in any practice setting.46 A validated screening tool can determine nutrition risk in all types of patients, including those with fluid shifts and for whom weight and height cannot be easily obtained.47,48 Validated tools should be quick and easy to use, reliable and valid, economical, of low risk to the individual being screened, and appropriate for the population and care setting.
Nutrition screening and rescreening should be conducted in accordance with the mandates outlined by accrediting bodies and a healthcare facility’s internal policies. In acute care facilities in the, nutrition screening is conducted within 24 hours of admission. Information collected through the screen is used by a registered dietitian nutritionist (RDN) to identify patients whose nutrition concerns warrant further assessment. In long-term postacute care, nutrition screening is completed at regular intervals based on the Minimum Data Set regulations. In all care settings, communication with the RDN is essential to determine appropriate intervention(s) and discuss opportunities to improve patient outcomes.
Many nutrition risk screening parameters are common in assigning risk level. These include height and weight, unintentional weight changes, changes in intake/appetite, lifestyle habits (physical activity, tobacco use), gastrointestinal disorders, and medical history. Laboratory data are not used in traditional nutrition screens, and serum proteins such as albumin and prealbumin are not endorsed for nutrition screening.49 There is no association between increased or decreased protein intake and changes in these markers. As a result, nutrition screening or assessment based on serum protein levels is not recommended.46
Nutrition Screening Tools
Common nutrition screening instruments include the Mini Nutritional Assessment (MNA), Malnutrition Universal Screening Tool, Nutrition Risk Screening 2002, and the Short Nutritional Assessment Questionnaire.3,47,48,50–55 All of these screening tools have been validated for identifying nutrition risk.
For example, Grattagliano and colleagues50 used the MNA to screen 274 patients 75 years or older in four towns in Southern Italy. They concluded that the easy-to-use screen allowed the four general practitioners involved in the study to quantify the risk for major events. Early identification of impaired nutrition status allowed for the timely development and implementation of interventions.50 Further, a prospective cohort study of 471 patients admitted to a medical center in Helsinki concluded that decreased nutrition status, as measured by the Malnutrition Universal Screening Tool score (OR, 3.825; 95% CI, 1.730-8.455; P = .001), is one of the best predictors for the development of PIs in older adults.56 Finally, research data collected from 422 patients (average age, 85.0 ± 7.6 years) at a rural intermediate and acute care hospital in Japan imply that the MNA screen assisted in forecasting the development of PIs and that a score of less than 8 on the MNA is a better predictor for PIs than the Subjective Global Assessment, the Braden Scale, and plasma arginine levels. The results of these studies reinforce the need to conduct nutrition screens and assessments.57
NEONATES AND CHILDREN
As indicated in several studies, neonates and pediatric patients are also at risk of developing PIs. Multicenter studies report PI prevalence estimates from 0.47% to 35%, with the highest rates occurring in ICUs.58,59 Schlüer and colleagues59 estimated a 43% PI incidence in their neonatal ICU. Most pediatric PIs are facility acquired,60 and medical devices account for the highest number of PIs in neonates and young children.58,61
Pediatric PIs are also expensive. A study by Goudie et al62 reported the average cost for patients aged 1 to 4 years was $20,000 per PI. This increased to $85,803 when multiplied by the available prevalence and incidence data.62
Pediatric malnutrition leads to complex hospital stays because of the complications from underlying diseases and conditions such as slow wound healing. In these patients, this contributes to increased hospital costs and length of stay.63 The ASPEN defines pediatric malnutrition (undernutrition) as “an imbalance between nutrient requirement and intake, resulting in cumulative deficits of energy, protein or micronutrients that may negatively affect growth, development and other relevant outcomes.”64 Many factors are involved in defining pediatric malnutrition including illness, injury, and adverse environmental or behavioral conditions. The Academy of Nutrition and Dietetics and ASPEN’s consensus statement on the indicators of pediatric malnutrition (undernutrition) for ages 1 month to 18 years recommends that a standardized set of diagnostic indicators be used to identify and document undernutrition in routine pediatric practice. The recommended indicators include z scores for weight for height/length, BMI for age, length/height for age, or mid-upper arm circumference when a single datum is available.65 When two or more data points are available, indicators may also include weight gain velocity (<2 years of age), weight loss (2-20 years of age), deceleration in weight for length/height z score, and inadequate food nutrient intake.65
Neonates and pediatric patients are at risk of compromised nutrient intake because of an increased nutrition requirement per unit weight to meet their normal growth needs, along with smaller appetites. Children at risk of and with PIs usually have other comorbidities that compromise their ability to consume adequate nutrients to promote and maintain wound healing.66 Early nutrition screening and assessment are important to identify malnutrition risk and implement a care plan. The EPUAP/NPIAP/PPPIA CPG recommends providers conduct an age-appropriate nutritional screen and assessment for neonates and children at risk of PIs (Table 1).1 There are various screening tools used for this population, including the Subjective Global Nutritional Assessment for Children, the Pediatric Nutritional Risk Score, the Screening Tool for the Assessment of Malnutrition in Pediatrics, Pediatric Yorkhill Malnutrition Score, and the Screening Tool for the Risk of Impaired Nutritional Status and Growth.
Growth assessment is the strongest gauge of nutrition status in pediatric patients and neonates. Anthropometric data including weight, height, growth scores, head circumference, and Z scores are used to determine if a neonate or child is developing according to established parameters. Z scores are the preferred nutrition assessment tool because they are more descriptive than growth charts.66,67
As part of the nutrition assessment, the RDN may conduct a nutrition-focused physical examination to determine micronutrient deficiencies and signs of malnutrition. They should conduct weekly nutrition assessments for critically ill children.68–70 The healthcare team, including the RDN and pediatrician, should devise an individualized nutrition plan for the pediatric patients, and it should include the mode of feeding, frequent monitoring of intake and growth status, oral supplements, nutrition support, and feeding strategies for parents and caregivers.67,71
The EPUAP/NPIAP/PPPIA CPG recommends the completion of a comprehensive nutrition assessment for adults at risk of PIs and malnutrition, as well as for all adults with a PI (Table 1).1 A pre/post quasi-experimental design study conducted in Florida examined the use of an interprofessional nutrition protocol on 100 patients 60 years or older with Stage 2 and/or 3 PIs. This study concluded that conducting a nutritional assessment is linked to increased PI healing rates.72 Completing a nutrition assessment is a component of the Nutrition Care Process. Developed by the Academy of Nutrition and Dietetics and adopted by countries around the world, this process includes four basic steps: nutrition assessment, diagnosis, interventions, and plan monitoring and evaluation.
The nutrition assessment should be completed by an RDN in collaboration with the interprofessional nutrition team.72 The assessment includes the interpretation of anthropometric, biochemical, clinical, and dietary data.73 Information obtained and analyzed should include food/nutrition-related history, biochemical data, medical tests and procedures, anthropometric measurements, nutrition-focused physical findings, and patient history.73 The food/nutrition-related history domain includes assessment parameters such as food and nutrient intake, medication and complementary/alternative medication use, factors affecting food and nutrition supplies, and physical activity. Anthropometric measurements include height, weight, body frame, weight change, body mass, growth pattern indices, and body compartment estimates. Nutrition-focused physical findings include muscle and subcutaneous fat atrophy, oral health, swallowing function, and appetite. Patient history includes a personal, medical, social, and health history.73
Body composition is an independent risk factor for malnutrition, sarcopenia, and associated comorbidities. Very often, patients who are overweight or obese are described in the medical records as “well nourished.” Taking a closer look at the body composition of these individuals over time can show decreased body mass, uncovering an increased risk for sarcopenic obesity. In addition, sarcopenia is also often present in (immobile) individuals with undernutrition.
Again, although they support the use of laboratory data such as albumin and prealbumin to establish the overall prognosis of the patient, these values are not sensitive indicators of nutrition status. Serum protein levels can be affected by inflammation, renal function, hydration, and other factors.49,74–77
NUTRITION CONSIDERATIONS FOR PREVENTION AND HEALING
The EPUAP/NPIAP/PPPIA CPG recommendation is to provide 30 to 35 kcal/kg of body weight per day for adults with a PI who are malnourished or at risk of malnutrition. The recommendation for protein is 1.25 to 1.5 g/kg of body weight per day.1
Providing and consuming adequate kilocalories support collagen and nitrogen synthesis, thus promoting anabolism by sparing protein from being used as an energy source. Fat is the most concentrated source of calories, providing a reserve source of energy in the form of stored triglycerides in adipose tissue. It cushions bony prominences, provides insulation, and transports the fat-soluble vitamins A, D, E, and K, which are stored in the liver.
If the energy from carbohydrates and fat fails to meet the individual’s needs, the liver and kidneys synthesize glucose from noncarbohydrate sources, such as protein. The body uses this released energy as fuel for anabolism, which increases the body’s metabolic rate and caloric requirements. Wound healing is compromised if the body is forced to produce glucose by degrading protein and depleting lean body mass (LBM). The decline in LBM can lead to muscle wasting, decline in subcutaneous fat, and poor PI healing. Demling’s78 research noted that any loss of LBM is detrimental, but with a 20% loss, the competition between using protein to rebuild LBM and wound healing is equal, therefore slowing the healing process. This study recommended increasing energy intake 50% above the normal level and increasing protein to 1.5 g/kg of body weight.78
Because there is no specific research on optimal caloric requirement to prevent PIs, the EPUAP/NPIAP/PPPIA CPG suggests that energy and protein intake be optimized for the individual. This should be done within the context of the individual’s nutrition status (eg, current, usual, and goal weights) and clinical condition.
The EPUAP/NPIAP/PPPIA CPG also provides specific guidance on the energy needs of patients with PIs (Table 1). In a meta-analysis of observational studies, Cereda et al79 reported that the use of indirect calorimetry to measure resting energy expenditure using a correction factor of 1.3 for physical activity (for individuals confined to bed) and a 1.1 PI correction factor adds to a total daily energy requirement of about 30 kcal/kg per day.79 Ohura et al80 reported that, in hospitalized older adults receiving tube feeding (n = 60), 12 weeks of nutrition support calculated using resting energy expenditure × activity factor 1.1 × stress factor 1.3 to 1.5 (mean intake, 37.9 ± 6.5 kcal/kg per day) was associated with reduced PI size (P < .001) and depth (P < .05) compared with standard care (mean intake, 29.1 ± 4.9 kcal/kg per day).
The energy and protein needs of pediatric patients are also increased when they experience the metabolic stress of healing wounds. Their caloric and protein requirements should be assessed frequently to avoid over or under feeding. The RDNs and clinicians assessing and estimating nutrition needs for the pediatric population can refer to the Academy of Nutrition and Dietetics Pediatric Nutrition Care Manual and the Pediatric Pocket Guide to Nutrition Assessment for guidance.
Protein is vital for the growth and maintenance of cells, fluid balance, and blood clotting; its functions include immune function preservation, wound healing enzyme repair and synthesis, cell multiplication, and collagen and connective tissue synthesis. Additional protein is also required to compensate for the nitrogen losses that occur with PI exudate.
Research supports the theory that increased protein levels are linked to improved PI healing. As early as 1993, Breslow et al81 demonstrated that individuals receiving higher-protein/higher-calorie diets had a statistically greater reduction in PI surface area compared with baseline than the individuals receiving a standard diet (P < .02). A change in PI surface area was correlated with both dietary protein (r = 0.50, P < .01) and energy intake (r = −0.41, P < .03).81 A randomized controlled trial (RCT) by Ohura et al80 stated that a high intake of protein can result in reducted PI size and depth compared with a low protein intake. An RCT by Lee et al82 reported that providing a standard diet with a concentrated protein supplement equaling 45 g daily resulted in a 60% reduction in Pressure Ulcer Scale for Healing scores after 8 weeks of treatment, whereas standard care and a placebo resulted in a 48% reduction (P < .05). Yamamoto et al35 demonstrated improvement in PI healing when adults consumed more than 30 kcal/kg of body weight per day, whereas individuals consuming ≤20 kcal/kg of body weight per day experienced deterioration or no improvement in healing. Finally, in a trial by Ohura et al80 comparing the efficacy of two different nutrition regimens, high-calorie (37.9 ± 6.5 vs 29.1 ± 4.9 kcal/kg per day) and high-protein intake (intake 1.62 ± 0.30 vs 1.24 ± 0.22 g/kg per day) resulted in improved PI healing (higher reduction in area and depth). A secondary analysis of the same trial data demonstrated that high-calorie, high-protein support in patients with PIs is a cost-effective intervention.83
The recommended dietary allowance for protein for all adults, including older adults, is 0.8 g/kg of body weight. Evidence supports that LBM is maintained when an older adult consumes higher levels of protein, in the range of 1.0 to 1.2 g/kg per day.84–86 Evidence also supports increasing energy and protein intake for adults and children with PIs who are malnourished or at risk of malnutrition.84–86
An adult’s body is 60% water, which is distributed in the intracellular, interstitial, and intravascular compartments. It serves as the transport medium for moving nutrients to the cells and removing waste products. Water is the solvent for minerals, vitamins, amino acids, glucose, and other small molecules, allowing them to diffuse into and out of cells.
The EPUAP/NPIAP/PPPIA CPG recommends providers encourage adequate fluid intake. Although current research has not determined the optional formula for calculating a daily fluid requirement for individuals with PIs, 1 mL fluid/kcal consumed is commonly used.62,54,87 Adequate daily fluids/water should be offered to and encouraged for all individuals with PIs. Those with draining wounds, emesis, diarrhea, elevated temperature, or increased perspiration require additional fluids/water to replace lost fluid.88 Clinicians should monitor individuals for any signs or symptoms of dehydration: changes in weight, skin turgor, urine output, or elevated serum sodium. Older adults usually have increased body fat and decreased LBM, thus decreasing the percentage of water their bodies can store. This, combined with a decreased sense of thirst, increases their risk of dehydration.88 Fluid requirements are met with liquids, including the water content of food, which accounts for 19% to 27% of the total fluid intake of healthy adults.
As explained in Table 3, micronutrients play a role in the PI healing process and are key components of a healthy diet. Previously, megadoses of supplements such as ascorbic acid and zinc have been prescribed for patients with PIs. Because of the lack of evidence-based research on the validity of this practice, the 2019 Guideline committee did not study this issue. Many of the oral supplements, enteral formulas, and fortified foods recommended for individuals with PIs contain additional micronutrients and should be considered before recommending additional supplementation.
THE ROLE OF SUPPLEMENTS
Evidence-based guidelines, particularly those focusing on nutrition in older populations, have highlighted that despite many trials the most effective treatment options for malnutrition still need to be identified. Therefore, approaches should be comprehensive, relying first on improving oral intake.89,90 Prior to or in addition to offering oral nutrition supplements, clinicians should consider comprehensive approaches for improving oral intake:
- nutrition counseling
- modifying food, such as with fortified foods
- revising/modifying or liberalizing diet restrictions that result in decreased intake91
- offering assistance with eating
- honoring cultural/religious food preferences
- providing a pleasant eating environment
As reported above, a positive energy and protein balance to sustain anabolism plays a crucial role in skin viability and wound healing. However, patients with chronic diseases or at risk of/with a PI frequently cannot meet protein and calorie needs. Aside from increasing the energy expenditure of the patient, PIs are responsible for a further worsening the energy balance.79 When oral feeding is safe, the use of oral nutritional supplements (ONSs) can be an effective strategy to help fulfill protein and calorie requirements.
The EPUAP/NPIAP/PPPIA CPG recognizes the role of supplements and recommends ONSs with micronutrients for individuals with a PI who are malnourished (or at risk; Table 1). According to a systematic review of RCTs, ONSs are usually well tolerated and result in both a positive energy balance and clinical benefits, especially when higher-energy-density ONSs (1.5-2.4 kcal/mL) are consumed between meals.92 Because ONSs include products that supply macro- and micronutrients, providers must weigh their value for the treatment plan. Health professionals are advised to review the nutrition labeling to determine nutrient adequacy.
Studies investigating the role of ONSs in preventing PIs have mixed findings, with uncertainty surrounding their efficacy. All of the investigations included in the guideline review were conducted in older populations in which PIs are clearly of multifactorial origin, and the contribution of ONSs is more difficult to establish because it is only one part of the overall patient’s care, which is oriented toward treating all underlying conditions. Further, the heterogeneity in study designs contributed to the risk of bias.5,6,93–96 However, a meta-analysis of trials in this area found that the provision of high-calorie (250-500 kcal) high-protein ONSs is associated with a 25% lower incidence of PIs in individuals at risk compared with routine care (OR, 0.75; 95% CI, 0.62-0.89).97
On the other hand, evidence on the efficacy of ONSs in increasing the rate of healing is consistent and substantiated by different trials, which also suggest that the duration of intervention should be at least 4 weeks and reasonably up to complete healing. These studies support not only the importance of extra energy and protein but also the positive effect adding arginine and micronutrients (zinc and antioxidants).5,81,82,98–101 A recent large double-blind RCT (the Oligo Element Sore Trial) has elucidated the independent role of these additional nutrients in PI healing.100,102 In this study, high-energy, high-protein ONSs (two bottles per day; 500 kcal and 40 g protein) enriched with arginine, zinc, and antioxidants were compared with isocaloric, isonitrogenous control ONSs in malnourished adults with Stages 2 through 4 (70% Stage 3 or 4) PIs. After 8 weeks, a greater reduction in wound surface area was achieved in the intervention group (adjusted mean change, 18.7%; 95% CI, 5.7-31.8). Interestingly, a reduced intensity of care (fewer dressings and less time spent changing them) has been reported with the use of this formula.103
Last but not least, using data from available RCTs, Australian researchers have demonstrated that nutrition support is a cost-effective intervention in preventing PIs in the hospital setting. Specifically, ONSs are likely responsible for a reduction in length of hospital stay when compared with usual care (standard diet).104–106 Analysis of the Oligo Element Sore Trial data also showed that the studied ONS is a cost-effective treatment associated with substantial savings when compared with the control formula.99 With this background, the use of ONSs in preventing and treating PIs could be recommended.
Despite limited evidence supporting artificial nutrition and hydration for PI intervention and treatment, the interprofessional team should discuss the risks and benefits of enteral nutrition (EN; tube feeding) or parenteral nutrition (PN) with individuals who cannot meet their nutrition requirements through oral intake despite previous intervention. The interdisciplinary team should consider if the patient has the desire and/or capacity to tolerate nutrition support. Nutrition goals should not take priority over the patient-centered goals of the individual.
One low-quality level 1 study and three low-quality level 3 studies indicate that the provision of EN and PN has limited impact on preventing PI for those at risk.94,95,107,108 The high-acuity level of patients in acute or long-term care increases the incidence of PIs and can lead to the decision to trial EN or PN. The long-term care patients in Arinzon and colleagues’107 study receiving EN were at greater risk of developing PI and had lower BMIs than those who were not. Considering the length of the trials (from 2 to 12 weeks), lack of reported comorbidities, and quality of the trials, it remains unclear whether offering artificial nutrition and hydration for those at risk of PIs would reduce prevalence.
The goal for artificial nutrition support for individuals with PIs is to improve their nutrition status, promote healing, and restore their immune function.109,110 When PI healing has stalled and oral intake is inadequate to support healing, EN should be considered if it is consistent with the individual’s goals of care. The RDN and interprofessional team should evaluate the patient’s medical condition to determine whether EN is a long- or short-term solution. Prior to initiating EN, the risks and benefits of nutrition support must be discussed with the patient and/or caregivers. Although artificial nutrition and hydration are medical treatments, an individual’s cultural and/or religious values may dictate their decision to accept or decline EN.
If the gastrointestinal tract is functioning, EN is the preferred route. Parenteral nutrition should be considered for patients whose nutrition requirements cannot be met with EN. Prior to the initiation of EN, the RDN should assess the patient’s calorie, protein, and hydration needs and tailor the feeding regimen to meet their needs. There are pediatric enteral formulas designed for children from 1 to 13 years of age. These formulas meet the recommended dietary reference intakes for children aged 1 to 8 years in 1,000 mL/d and 1,500 mL/d for children aged 9 to 14 years.111
After artificial nutrition support is initiated, the interprofessional team should frequently evaluate the patient’s tolerance to EN and note any adverse reactions such as nausea, diarrhea, or vomiting. Clinicians should also routinely check and confirm that the patient is receiving the correct formula in the prescribed amount. The RDN and interprofessional team should document the benefit from the feedings in relation to the desired outcome of healing and stabilizing nutrition status in the medical record. They should also monitor and evaluate the individual’s tolerance and progress toward achieving the desired outcome and recommended changes as needed.
Research reviewing EN for improved outcomes for PI healing is limited. Two high-level studies, one with 60 individuals and another with 28, noted improvement in healing rates when the nutrition support used was a high-protein, disease-specific formula.80,102 Arinzon and colleagues’107 study of residents with dementia residing in long-term care reported more complications, such as pneumonia, weight loss, and death, in the intervention group receiving EN than those receiving an oral diet (61% vs 34%, P < .01). Another study reported no change in mortality with PN over EN in critically ill individuals.112
Patients receiving palliative care are at high risk of developing PIs because they have a serious illness, are immobile, or are approaching end of life. The EPUAP/NPIAP/PPPIA CPG highlights the importance of discussing benefits and harms of EN or PN with individuals in palliative care and their families and/or caregivers (Table 1).
The guiding principles of palliative care for PI management focus on relieving pain and providing comfort for the individual. Nutrition interventions should be compatible with patient goals and desired outcomes. For example, serving the individual’s favorite food or beverage when requested improves his or her quality of life.
It is the position of the Academy of Nutrition and Dietetics that “individuals have the right to request or refuse nutrition and hydration as medical treatment,”113 and ESPEN states that a “competent patient has the right to refuse a treatment after adequate information even when this refusal would lead to his or her death.”114 Hospice PI treatment goals should be individualized, respecting each person's unique values and personal decisions.115
CARE PLANNING, PATIENT MONITORING, AND EVALUATION
Regardless of the setting, the EPUAP/NPIAP/PPPIA CPG recommends that an individualized nutrition care plan be developed. The interdisciplinary team is responsible for nutrition care that addresses the desired outcomes for the individual. Allen’s72 study demonstrated that individualized nutrition assessment and planning for older adults with Category/Stage 2 or 3 PIs (n = 100) are associated with improved wound healing compared with standardized nutrition plans (37% vs 23.4%, P < .05). The care plan process should encompass the policies and/or regulations of the organization. The RDN builds the nutrition care plan based on the information gathered in the nutrition assessment, including data generated by the physician; nurses; and physical, occupational, and speech language therapists. The patient-centered care plan should
- be individualized
- involve the individual and all disciplines
- reflect the patient’s choices/preferences
- offer a variety of interventions to meet the stated goal
- identify specific interventions
- educate the individual/caregiver on the benefits of the suggested intervention
- include a time frame for completion or review
- be documented in the medical record
The interprofessional team should counsel individuals and suggest a variety of other options for patients residing in the community who cannot prepare meals or afford ONSs and vitamin/mineral supplements. Suggestions include eating small, frequent meals and snacks such as high-calorie bars, sandwiches, Greek yogurt, homemade milk shakes, instant breakfasts, and other nutrient-rich items.46 Referral to an RDN for individualized counseling would be advantageous for community-dwelling patients with literacy or language difficulties. Some US hospitals host a Food Pharmacy including ONSs for individuals who have limited access to affordable and nutritious foods. Wound care clinics and rehabilitation departments, acute care hospitals, and post-acute care facilities are encouraged to provide hot and cold beverages as part of their hydration protocols and/or to make strategic connections with a Food Pharmacy program.
Routine or periodic monitoring of the care plan is the most important component of the nutrition care process. Interventions must be adjusted with any change in conditions and when progress toward the desired outcome is not achieved. The RDN may need to reassess the patient or refer them to another discipline for further evaluation or treatment (Figure 1).
PATIENT EDUCATION AND ENGAGEMENT
Patient education and engagement are an important component of nutrition assessment and treatment for all individuals, including those with or at risk of PIs.1 Evidence on the effectiveness of education in reducing PI incidence and promoting healing has shown mixed results; however, there was sufficient evidence for the EPUAP/NPIAP/PPPIA CPG to recommend providing individuals with or at risk of PIs access to education, skills training, and psychosocial support. The evidence indicates that for individuals with ongoing PI risk (eg, those with spinal cord injury), multifaceted lifestyle skills programs or telephone-based education and support programs can produce short-term positive impacts on knowledge, education, and quality of life.116–119 Patients themselves have noted the importance of engaging in nutrition education. Haesler et al120,121 reported that 71.8% (275/383) of respondents to an international survey identified that knowing more about what to eat and drink to prevent PI and to maintain healthy skin was important or very important in caring for themselves. Further, the survey respondents identified that nutrition education was also important for their family and caregivers.
Given the complexities of nutrition for individuals with and at risk of PIs, education and nutrition-related lifestyle coaching (eg, guidance on weight management, menu planning, food selection and preparation) are an important component to include in patient and family education and engagement programs.120,121 Written information on nutrition should be presented in a concise manner to reinforce person-to-person education. Hartigan et al122 noted that providing a simple pamphlet with evidence-based PI-related messages, including “Eat plenty of protein (e.g. meat, fish, eggs)” to a sample of community-based older adults at risk of PI (n = 75) was associated with improvements in knowledge of PI risk factors. A similar concise written resource was used by Chaboyer et al123 as a part of a comprehensive PI prevention bundle delivered in eight Australian hospitals. The simple nutrition message provided to patients was “Eat a healthy diet.” The hazard ratio (0.48; 95% CI, 0.20-1.21) indicated a 52% reduction in hospital-acquired PIs associated with the intervention. In this acutely ill population, the researchers noted that the willingness of individuals to engage in education interventions is limited by their clinical condition.123 This suggests that appropriate timingis an important consideration for nutrition-related education.
Nutrition plays a vital role in human growth and development; the maintenance of good health and functionality; prevention and treatment of infectious, acute, and chronic diseases; and PI development and treatment. To effectively and efficiently advance the role of nutrition in improving and sustaining health and tissue viability to prevent or treat PI, efforts must be made to advance nutrition research.
Improved nutrition could be one of the most cost-effective approaches to address many of the societal, environmental, and economic challenges facing nations around the world today.124 Adequate nutrition promotes positive outcomes among patients at risk of or with PIs in all care settings. Key research priorities on nutrition and PI prevention and treatment include the impact of malnutrition, frailty, and sarcopenia on patient recovery. Methods to estimate calories and protein requirements for individuals classified as obese need to be defined. Patient history, including personal, medical, social, and health history, also influences PI development. Research on the use of high-calorie, high-protein ONSs as an intervention to reduce the incidence of PI is needed, along with studies on key nutrients such as amino acids, zinc, and antioxidants as adjunct therapy. The value and benefits of EN and PN, either supplemental or total, should also be clarified. Finally, the cost-effectiveness of nutrition interventions in patients with PIs must always be considered among the outcomes of interest.
Nutrition is an important consideration when treating patients at risk of or with PIs. Early nutrition screening using a validated tool and assessment is a key element in diagnosing malnutrition, which can impede healing. The interdisciplinary team including the RDN should apply the CPG recommendations to reduce process variation and achieve positive outcomes.
- Use a validated nutrition screening tool to identify the nutrition status of individuals at risk of or with PIs.
- Refer individuals at risk of or with PIs to an RDN or other qualified professional for a nutrition assessment and collaborate with the interprofessional team and patient to determine a patient-centered nutrition plan.
- Encourage consumption of a balanced diet based on individualized requirements. Supplement between meals if needed to achieve assessed requirements.
- Offer nutrition support to individuals who cannot consume adequate intake, assuming this is compatible with individual’s goals and wishes.
1. European Pressure Ulcer Advisory Panel, National Pressure Injury
Advisory Panel, and Pan Pacific Pressure Injury
Alliance. Prevention and Treatment of Pressure Ulcers/Injuries: Clinical Practice Guideline. The International Guideline. 3rd ed. Haesler E, ed. 2019. http://internationalguideline.com
. Last accessed December 27, 2019.
2. Keller HH, Goy R, Kane SL. Validity and reliability of SCREEN II (Seniors in the Community: Risk Evaluation for Eating and Nutrition
, version II). Eur J Clin Nutr 2005;59(10):1149–57.
3. Neelemant F, Kruizenga HM, de Vet HC, Seidell JC, Butterman M, van Bokhorst-de van der Schueren MA. Screening malnutrition
in hospital outpatients. Can the SNAQ malnutrition
tool also be applied to this population? Clin Nutr 2008;27(3):439–46.
4. Nestle Nutrition
Institute. Mini Nutritional Assessment
MNA®. 1994. www.mna-elderly.com/forms/mini/mna_mini_english.pdf
. Last accessed December 27, 2019.
5. Ek AC, Unosson M, Larsson J, von Schenck H, Bjurulf P. The development and healing of pressure sores related to the nutritional state. Clin Nutr 1991;10(5):245–50.
6. 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. Nutrition
7. Berlowitz DR, Wilking SV. Risk factors for pressure sores. A comparison of cross-sectional and cohort-derived data. J Am Geriatr Soc 1989;37(11):1043–50.
8. Brandeis G, Ooi W, Hossain M, Morris J, Lipsitz L. A longitudinal study of risk factors associated with the formation of pressure ulcers in nursing homes. J Am Geriatr Soc 1994;42:388–93.
9. Dhandapani M, Dhandapani S, Agarwal M, Mahapatra AK. Pressure ulcer in patients with severe traumatic brain injury: significant factors and association with neurological outcome. J Clin Nurs 2014;23(7-8):1114–9.
10. Ham HW, Schoonhoven LL, Schuurmans MM, Leenen LL. Pressure ulcer development in trauma patients with suspected spinal injury: the influence of risk factors present in the emergency department. Int Emerg Nurs 2017;30:13–9.
11. Bergstrom N, Braden B. A prospective study of pressure sore risk among institutionalized elderly. J Am Geriatr Soc 1992;40(8):747–58.
12. Bergquist S, Frantz R; Pressure ulcers in community-based older adults receiving home health care. Prevalence, incidence, and associated risk factors. Adv Wound Care 1999;12(7):339.
13. Compton F, Hoffmann F, Hortig T, et al. Pressure ulcer predictors in ICU patients: nursing skin assessment
versus objective parameters. J Wound Care 2008;17(10):417.
14. De Laat E, Pickkers P, Schoonhoven L, Verbeek A, Feuth T, van Achterberg T. Guideline implementation results in a decrease of pressure ulcer incidence in critically ill patients. Crit Care Med 2007;35(3):815–20.
15. Defloor T, Grypdonck M. Pressure ulcers: validation of two risk assessment
scales. J Clin Nurs 2005;14(3):373–82.
16. Kwong EW-y, Pang SM-c, Aboo GH, Law SS-m. Pressure ulcer development in older residents in nursing homes: influencing factors. J Adv Nurs 2009;65(12):2608–20.
17. Roca-Biosca A, Velasco-Guillen M, Rubio-Rico L, García-Grau NA, Anguera-Saperas L. Pressure ulcers in the critical patient: detection of risk factors. Enferm Intensiva 2012;23(4):155–63.
18. Serpa L, Santos V. Assessment
of the nutritional risk for pressure ulcer development through Braden Scale. JWOCN 2007;34(3S):S4–S6.
19. Watts D, Abrahams E, MacMillan C, et al. Insult after injury: pressure ulcers in trauma patients. Orthop Nurs 1998;17(4):84–91.
20. Coleman S, Smith IL, McGinnis E, et al. Clinical evaluation of a new pressure ulcer risk assessment
instrument, the Pressure Ulcer Risk Primary or Secondary Evaluation Tool (PURPOSE T). J Adv Nurs 2017;23:23.
21. National Institute for Health and Clinical Excellence. Pressure ulcers: prevention and management clinical guideline [CG179]. www.nice.org.uk/guidance/cg179
. 2014. Last accessed December 27, 2019.
22. Norton D, Exton-Smith AN, McLaren R. An Investigation of Geriatric Nursing Problems in Hospital. London, UK: National Corporation for the Care of Old People; 1962.
23. Waterlow J. A risk assessment
card. Nurs Times 1985;81:24–7.
24. Bergstrom N, Braden BJ, Laguzza A, Holman V. The Braden Scale for predicting pressure sore risk. Nurs Res 1987;36(4):205–10.
25. Cubbin B, Jackson C. Trial of a pressure area risk calculator for intensive therapy patients. Intensive Care Nurs 1991;7:40–4.
26. Vocci MC, Toso LAR, Fontes CMB. Application of the Braden Q Scale at a pediatric intensive care unit. Rev Enferm UFPE 2017;11(1):165–72.
27. Cederholm T, Barazzoni R, Austin P, et al. ESPEN guidelines on definitions and terminology of clinical nutrition
. Clin Nutr 2017;36:49–64.
28. Basics in Clinical Nutrition
. 4th ed. Sobotka Led. Czech Republic: Galen; 2012.
29. Cederholm T, Jensen GL, Correia MITD, et al. GLIM criteria for the diagnosis of malnutrition
—a consensus report from the global clinical nutrition
community. Clin Nutr 2019;38(1):1–9.
30. Fry DE, Pine M, Jones BL, Meimban RJ. Patient characteristics and the occurrence of never events. Arch Surg 2010;145(2):148–51.
31. Green CJ. Existence, causes and consequences of disease-related malnutrition
in the hospital and the community and clinical and financial benefits of nutritional intervention. Clin Nutr 1999;18(suppl. 2):3–28.
32. Iizaka S, Okuwa M, Sugama J, Sanada H. The impact of malnutrition
-related factors on the development and severity of pressure ulcers in older patients receiving home care. Clin Nutr 2010;29(1):47–53.
33. Verbrugghe M, Beeckman D, van Hecke A, et al. Malnutrition
and associated factors in nursing home residents: a cross-sectional, multi-centre study. Clin Nutr 2013;32(3):438–43.
34. Wojcik A, Atkins M, Mager DR. Dietary intake in clients with chronic wounds. J Can Diet Assoc 2011;72(2):77–82.
35. Yamamoto T, Fujioka, Kitamura R, et al. Evaluation of nutrition
in the healing of pressure ulcers: are the EPUAP nutritional guidelines sufficient to heal wounds? Wounds 2009;21(6):153–7.
36. 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(12):1549–54.
37. Banks M, Bauer J, Graves N, Ash S. Malnutrition
and pressure ulcer risk in adults in Australian health care facilities. Nutr Clin Pract 2010;26(9):896–901.
38. Crichton M, Craven D, Mackay H, Marx W, de van der Schueren M, Marshall S. A systematic review, meta-analysis and meta-regression of the prevalence of protein-energy malnutrition
: associations with geographical region and sex. Age Ageing 2019;48(1):38–48.
39. Guenter P, Malyszek R, Bliss DZ, et al. Survey of nutritional status in newly hospitalized patients with Stage III or Stage IV pressure ulcers. Adv Skin Wound Care 2000;13(4 Pt 1):164–8.
40. Mathus-Vliegen E. Nutritional status, nutrition
and pressure ulcers. Nutr Clin Pract 2001;16:286–91.
41. Saghaleini SH, Dehghan K, Shadvar K, Sanaie S, Mahmoodpoor A, Ostadi Z. Pressure ulcer and nutrition
. Indian J Crit Care Med 2018;22(4):283–9.
42. AMA House of Delegates Adapts Policy to Recognize Obesity as a Disease. 2013. https://obesitymedicine.org/ama-adopts-policy-recognize-obesity-disease
. Last accessed December 27, 2019.
43. Centers for Disease Control and Prevention. Adult obesity facts. 2018. www.cdc.gov/obesity/data/adult.html
. Last accessed December 27, 2019.
44. Greco JA 3rd, Castaldo ET, Nanney LB, et al. The effect of weight loss surgery and body mass index on wound complications after abdominal contouring operations. Ann Plast Surg 2008;61:235–42.
45. Academy of Nutrition
and Dietetics. Definition of Terms List. Definition of Terms Workgroup, Quality Management Committee. 2019. www.eatrightpro.org/-/media/eatrightpro-files/practice/scope-standards-of-practice/20190910-academy-definition-of-terms-list.pdf
. Last accessed December 27, 2019.
46. Academy of Nutrition
and Dietetics. Nutrition
Care Manual. 2019. www.nutritioncaremanual.org
. Last accessed December 27, 2019.
47. Kondrup J, Rasmussen HH, Hamberg I, Stanga Z. Nutritional risk screening
(NRS 2002): a new method based on an analysis of controlled clinical trials. Clin Nutr 2003;3:321–36.
48. Elia M, Zellipour L, Stratton RJ. To screen or not to screen for adult malnutrition
? Clin Nutr 2005;24(6):867–84.
49. White J. Consensus Statement: AND and ASPEN: characteristics recommended for the identification and documentation of adult malnutrition
(undernutrition). J Acad Nutr Diet 2012;112(5):730–8.
50. Grattagliano I, Marasciulo L, Paci C, Montanaro N, Portincasa P, Mastronuzzi T. The assessment
of the nutritional status predicts the long term risk of major events in older individuals. Eur Geriatr Med 2017;8(3):273–4.
51. Hengstermann S, Fischer A, Steinhagen-Thiessen E, Schulz RJ. Nutrition
status and pressure ulcer: what we need for nutrition screening
. JPEN 2007;31(4):288.
52. Langkamp-Henken B, Hudgens J, Stechmiller JK, Herrlinger-Garcia KA. Mini nutritional assessment
scores are associated with nutritional indicators in elderly people with pressure ulcers. J Am Diet Assoc 2005;105(10):1590–6.
53. Poulia KA, Yannakoulia M, Karageorgou D, et al. Evaluation of the efficacy of six nutritional screening
tools to predict malnutrition
in the elderly. Clin Nutr 2012;31(3):378–85.
54. Trans Tasman Dietetic Wound Care Group. Evidence
based practice guidelines for the nutritional management of adults with pressure injuries. 2011. www.aci.health.nsw.gov.au/__data/assets/pdf_file/0004/388237/13.-Trans-Tasman-Dietetic-Wound-Care-Group-Pressure-Injury-Guidelines-2011.pdf
. Last accessed December 27, 2019.
55. Tsai AC, Chang TL, Wang YC, Liao CY. Population-specific short-form mini nutritional assessment
with body mass index or calf circumference can predict risk of malnutrition
in community-living or institutionalized a people in Taiwan. J Am Diet Assoc 2010;110(9):1328–34.
56. Tsaousi G, Stavrou G, Ioannidis A, Salonikidis S, Kotzampassi K. Pressure ulcers and malnutrition
: results from a snapshot sampling in a university hospital. Med Princ Pract 2015;24(1):11–6.
57. Yatabe MS, Taguchi F, Ishida I, et al. Mini nutritional assessment
as a useful method of predicting the development of pressure ulcers in elderly inpatients. J Am Geriatr Soc 2013;61(10):1698–704.
58. Schlüer AB, Schols JMGA, Halfens RUG. Risk associated factors of pressure ulcers in hospitalized children over one year of age. J Spec Pediatr Nurs 2014;1:80–9.
59. Schlüer AB, Halfens RJ, Schols JGA. Pediatric pressure ulcer prevalence: a multicenter, cross-sectional, point-prevalence study in Switzerland. Ostomy Wound Manage 2012;58(7):18–31.
60. McLane KM, Boolout K, McCord S, McCann, Jefferson LS. The 2003 national pressure ulcer prevalence study and skin breakdown study, a multisite study. J Wound Ostomy Continence Nurs 2004;31(4):168–78.
61. Curley MAO, Hasbari NR, Quigley SM, et al. Predicting pressure injury
risk in pediatric patients: the Braden QD Scale. J Pediatr 2018;192:168–95.
62. Goudie A, Dynan L, Brady PW, Fieldston E, Brilli RJ, Walsh KE. Costs of venous thromboembolism, catheter-associated urinary tract infection, and pressure ulcers. Pediatrics 2015;136(3):432–9.
63. Hecht C, Weber M, Grote, et al. Disease associated malnutrition
correlates with length of hospital stay in children. Clin Nutr 2015;34(1):53–9.
64. Mehta N, Corkins M, Lyman B, et al. Defining pediatric malnutrition
: a paradigm shift towards etiology-related definitions. JPEN 2013;37(4):460–81.
65. Becker R, Carney LN, Corkins MR, et al. Consensus statement of the Academy of Nutrition
and Dietetics/American Society for Parenteral and Enteral Nutrition
: indicators recommend for the identification and documentation of pediatric malnutrition
(undernutrition). Nutr Clin Prac 2015;30(1):147–61.
66. Mehta N, Compher C, ASPEN Board of Directors. A.S.P.E.N. clinical guidelines: nutrition
support of the critically ill child. J Parenter Enteral Nutr 2009;33(3):260–76.
67. Ranade D, Collins N. Children with wounds: the importance of nutrition
. Ostomy Wound Manage 2011:14–24.
68. Joosten KF, Hulst JM. Nutritional screening
tools for hospitalized children: methodological considerations. Clin Nutr 2014;33(1):1–5.
69. Mehta NM, Skillman HE, Irving SY, et al. Guidelines for the provision and assessment
support therapy in the pediatric critically ill patient: Society of Critical Care Medicine and American Society for Parenteral and Enteral Nutrition
. JPEN 2017;41(5):706–42.
70. Skillman J, Wischmeyer P. Nutrition
therapy in critically ill infants and children. JPEN 2008;32(5):520–34.
71. Rodriguez-Key M, Alonzi A. Nutrition
, skin integrity, and pressure ulcer healing in chronically ill children: an overview. Ostomy Wound Manage 2007;53(6):56–62.
72. Allen B. Effects of a comprehensive nutritional program on pressure ulcer healing, length of hospital stay, and charges to patients. Clin Nurs Res 2013;22(2):186–205.
73. Academy of Nutrition
and Dietetics. Electronic Nutrition
Care Process Terminology. 2019. www.ncpro.org
. Last accessed December 27, 2019.
74. Field LB, Hand RK. Differentiating malnutrition nutrition screening
: a nutrition
care process perspective. J Acad Nutr Diet 2015;15:824–8.
75. Fuhrman MP, Charney P, Mueller CM. Hepatic proteins and nutrition assessment
. J Am Diet Assoc 2004;104(8):1258–64.
76. Hand RK, Murphy WJ, Filed LB, et al. Validation of the Academy/A.S.P.E.N. malnutrition
clinical characteristics. J Acad Nutr Diet 2016;116(5):856–63.
77. Tobert CM, Mott SL, Nepple KG. Malnutrition
diagnosis during adult inpatient hospitalizations: analysis of a multi-institutional collaborative database of academic medical centers. J Acad Nutr Diet 2018;118(1):125–31.
78. Demling RH. Nutrition
, anabolism, and the wound healing process: an overview. Eplasty 2009;9:e9.
79. Cereda E, Klersy C, Rondanelli M, Caccialanza R. Energy balance in patients with pressure ulcers: a systematic review and meta-analysis of observational studies. J Am Diet Assoc 2011;111:1868–76.
80. Ohura T, Nakajo T, Okada S, Omura K, Adachi K. Evaluation of effects of nutrition
intervention on healing of pressure ulcers and nutritional states (randomized controlled trial). Wound Repair Regen 2011;19(3):330–6.
81. Breslow RA, Hallfrisch J, Guy DG, Crawley B, Goldberg AP. The importance of dietary protein in healing pressure ulcers. J Am Geriatr Soc 1993;41(4):357–62.
82. Lee SK, Posthauer ME, Dorner B, Redovian V, Maloney MJ. Pressure ulcer healing with a concentrated, fortified, collagen protein hydrolysate supplement: a randomized controlled trial. Adv Skin Wound Care 2006;19(2):92–6.
83. Hisashige A, Ohura T. Cost-effectiveness of nutritional intervention on healing of pressure ulcers. Clin Nutr 2012;31(6):868–74.
84. Morley JE, Argiles JM, Evans WJ, et al. Nutritional recommendations for the management of sarcopenia. J Am Med Dir Assoc 2010;11(6):391–6.
85. Vikstedt T, Suominen MH, Joki A, et al. Nutritional status, energy, protein, and micronutrient intake of older service house residents. J Am Med Dir Assoc 2011;12(6):302–7.
86. Wolfe RR, Miller SL. The recommended dietary allowance of protein: a misunderstood concept. J Am Med Dir Assoc 2008;299(24):2891–3.
87. Clark M, Schols JMGA, Benati G, et al. Pressure ulcers and nutrition
: a new European guideline. J Wound Care 2004;13(7):267–72.
88. Schols JMGA, de Groot CP, van der Cammen TJ, Olde Rikkert MG. Preventing and treating dehydration in the elderly during periods of illness and warm weather. J Nutr Health Aging 2009;13(2):150–7.
89. Volkert D, Beck AM, Cederholm T, et al. Management of malnutrition
in older patients—current approaches, evidence
and open questions. J Clin Med 2019;4;8(7).
90. Volkert D, Beck AM, Cederholm T, et al. ESPEN guideline on clinical nutrition
and hydration in geriatrics. Clin Nutr 2018;38(1):10–47.
91. Dorner B, Friedrich EK. Position of the Academy of Nutrition
and Dietetics: individualized nutrition
approaches for older adults: long-term care, post-acute care, and other settings. J Acad Nutr Diet 2018;118(4):724–35.
92. Hubbard GP, Elia M, Holdoway A, Stratton RJ. A systematic review of compliance to oral nutritional supplements. Clin Nutr 2012;31(3):293–312.
93. Delmi M, Rapin CH, Bengoa JM, Delmas PD, Vasey H, Bonjour JP. Dietary supplementation in elderly patients with fractured neck of the femur. Lancet 1990;335(8696):1013–6.
94. Hartgrink HH, Wille J, Konig P, Hermans J, Breslau PJ. Pressure sores and tube feeding in patients with a fracture of the hip: a randomized clinical trial. Clin Nutr 1998;17(6):287–92.
95. Horn SD, Bender SA, Ferguson ML, et al. The National Pressure Ulcer Long-term Care Study: pressure ulcer development in long-term care residents. J Am Geriatr Soc 2004;52(3):359–67.
96. Houwing RH, Rozendaal M, Wouters-Wesseling W, Beulens JW, Buskens E, Haalboom JR. A randomised, double-blind assessment
of the effect of nutritional supplementation on the prevention of pressure ulcers in hip-fracture patients. Clin Nutr 2003;22(4):401–5.
97. Stratton RJ, Ek AC, Engfer M, et al. Enteral nutritional support in prevention and treatment of pressure ulcers: a systematic review and meta-analysis. Ageing Res Rev 2005;4(3):422–50.
98. Banks MD, Ross LJ, Webster J, et al. Pressure ulcer healing with an intensive nutrition
intervention in an acute setting: a pilot randomised controlled trial. J Wound Care 2016;25(7):384–92.
99. Cereda E, Klersy C, Andreola M, et al. Cost-effectiveness of a disease-specific oral nutritional support for pressure ulcer healing. Clin Nutr 2017;36(1):246–52.
100. Cereda E, Klersy C, Serioli M, Crespi A, D'Andrea F. A nutritional formula enriched with arginine, zinc, and antioxidants for the healing of pressure ulcers: a randomized trial. Ann Intern Med 2015;162(3):167–74.
101. Neyens J, Cereda E, Meijer EP, Lindholm C, Schols JMGA. Arginine-enriched oral nutritional supplementation in the treatment of pressure ulcers: a literature review. Wound Medicine 2017;16:46–51.
102. Cereda E, Gini A, Pedrolli C, Vanotti A. Disease-specific, versus standard, nutritional support for the treatment of pressure ulcers in institutionalized older adults: a randomized controlled trial. J Am Geriatr Soc 2009;57(8):1395–402.
103. Van Anholt R, Sobotka L, Meijer E, et al. Specific nutritional support accelerates pressure ulcer healing and reduces wound care intensity in non-malnourished patients. Nutrition
104. Banks MD, Graves N, Bauer JD, Ash S. Cost effectiveness of nutrition
support in the prevention of pressure ulcer in hospitals. Eur J Clin Nutr 2013;67(1):42–6.
105. Tuffaha HW, Roberts S, Chaboyer W, Gordon LG, Scuffham PA. Cost-effectiveness and value of information analysis of nutritional support for preventing pressure ulcers in high-risk patients: implement now, research later. Appl Health Econ Health Policy 2015;13(2):167–79.
106. Tuffaha HW, Roberts S, Chaboyer W, Gordon LG, Scuffham PA. Cost-effectiveness analysis of nutritional support for the prevention of pressure ulcers in high-risk hospitalized patients. Adv Skin Wound Care 2016;29(6):261–7.
107. Arinzon Z, Peisakh A, Berner YN. Evaluation of the benefits of enteral nutrition
in long-term care elderly patients. J Am Med Dir Assoc 2008;9(9):657–62.
108. Bourdel-Marchasson I, Dumas F, Pinganaud G, Emeriau JP, Decamps A. Audit of percutaneous endoscopic gastrostomy in long-term enteral feeding in a nursing home. Int J Qual Health Care 1997;9(4):297–302.
109. Wild T, Rahbamia A, Killner M, Sobotka L, Eberlein T. Basics in nutrition
and wound healing. Nutrition
110. Dryden SV, Shoemaker WG, Kim JH. Wound management and nutrition
for optimal wound healing. Atlas Oral Maxillofacial Surg Clin N Am 2013;21:37–47.
111. Malone A, Carney IN, Mays A eds. ASPEN Enteral Nutrition
Handbook. 2nd ed. Silver Springs, MD: American society for Parenteral and Enteral Nutrition
112. Boyce B. An ethical perspective on palliative care. J Acad Nutr Diet 2017;117(6):970–2.
113. O'Sullivan-Maillet J, Schwartz DB, Posthauer ME. Ethical and legal issues in feeding and hydration. J Acad Nutr Diet 2013;113(6):828–33.
114. Druml C, Ballmer PE, Druml W, et al. ESPEN guideline on ethical aspects of artificial nutrition
and hydration. Clin Nutr 2016;35(3):545–56.
115. Harvey SE, Parrott F, Harrison DA, et al. A multicentre, randomised controlled trial comparing the clinical effectiveness and cost-effectiveness of early nutritional support via the parenteral versus the enteral route in critically ill patients (CALORIES). Health Technol Assess 2016;20(28):1–143.
116. Rottkamp BC. An experimental nursing study: a behavior modification approach to nursing therapeutics in body positioning of spinal cord-injured patients. Nurs Res 1976;25(3):181–6.
117. Carlson M, Vigen CL, Rubayi S, et al. Lifestyle intervention for adults with spinal cord injury: results of the USC-RLANRC Pressure Ulcer Prevention Study. J Spinal Cord Med 2019;42(1):2–19.
118. Kim JY, Cho E. Evaluation of a self-efficacy enhancement program to prevent pressure ulcers in patients with a spinal cord injury. Jpn J Nurs Sci 2017;14(1):76–86.
119. Arora M, Harvey LA, Glinsky JV, et al. Telephone-based management of pressure ulcers in people with spinal cord injury in low- and middle-income countries: a randomised controlled trial. Spinal Cord 2017;55(2):141–7.
120. Haesler E, Cuddigan J, Kottner J, Carville K. Guideline Governance Group. International consumer engagement in guideline development: surveying patients in 30 countries. Presented at the 14th Guideline International Network (G-I-N) Conference; Manchester: 2018.
121. Haesler E, Cuddigan J, Kottner J, Carville K. Guideline Governance Group. International consumer engagement in pressure injury
/ulcer guideline development: global survey of patient care goals and information needs. Presented at the National Pressure Ulcer Advisory Panel 2019 Annual Conference; St Louis, MO; 2019.
122. Hartigan I, Murphy S, Hickey M. Older adults' knowledge of pressure ulcer prevention: a prospective quasi-experimental study. Int J Older People Nurs 2012;7(3):208–18.
123. Chaboyer W, Bucknall T, Webster J, et al. The effect of a patient centred care bundle intervention on pressure ulcer incidence (INTACT): a cluster randomised trial. Int J Nurs Stud 2016;64:63–71.
124. Ohlhorst S, Russell R, Bier D, et al. Nutrition
research to affect food and a healthy life span. J Nutr 2013;143(8):1349–54.