The_Role_of_Nutrition_for_Pressure_Injury.

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The_Role_of_Nutrition_for_Pressure_Injury.

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The Role of Nutrition for Pressure Injury Prevention and Healing: The 2019 International Clinical Practice Guideline Recommendations Nancy Munoz, DNC, MHA, RDN, FAND, Lecturer, University of Massachusetts Amherst, Amherst, Massachusetts, Assistant Chief, Nutrition and Food Service, VA Southern Nevada Healthcare System, Las Vegas, Nevada, Director, National Pressure Injury Advisory Panel Mary Ellen Posthauer, RDN, LD, FAND, President, MEP Healthcare Dietary Services, Inc, Evansville, Indiana, Past President, National Pressure Injury Advisory Panel Emanuele Cereda, MD, PhD, Physician and Research Scientist, Clinical Nutrition and Dietetics Unit, Fondazione IRCCS Policlinico San Matteo, Pavia, Italy Jos M. G. A. Schols, MD, PhD, Professor of Old Age Medicine, Department of Family Medicine, Maastricht University, Limburg, the Netherlands Emily Haesler, PhD, BN, P Grad Dip Adv Nurs, Associate Professor, School of Nursing, Midwifery and Paramedicine, Curtin University, Perth, Australia

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GENERAL PURPOSE: To review the nutrition-related recommendations presented in the 2019 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 with further discussion of nutrition for pressure injury management in the context of the recommendations. TARGET AUDIENCE: This continuing education activity is intended for physicians, physician assistants, nurse practitioners, and nurses with an interest in skin and wound care. LEARNING OBJECTIVES/OUTCOMES: After participating in this educational activity, the participant should be better able to: 1. Distinguish nutrition and malnutrition, especially as they relate to the development and healing of pressure injuries. 2. Differentiate the tools and techniques that help clinicians assess nutrition status as well as the causes of pressure injuries in specific populations. 3. Identify interventions for improving nutrition status and promoting pressure injury healing.

ABSTRACT Macro- and micronutrients are required by each organ system in specific amounts to promote the growth, development, maintenance, and repair of body tissues. Specifically, nutrition plays an important role in the prevention and treatment of pressure injuries. The purpose of this manuscript is to review the nutrition-related recommendations presented in the 2019 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. Nutrition for pressure injury management is discussed in the context of the recommendations. KEYWORDS: assessment, clinical practice guidelines, evidence, malnutrition, nutrition, pressure injury, screening

ADV SKIN WOUND CARE 2020;33:123–36.

DOI: 10.1097/01.ASW.0000653144.90739.ad

unoz has disclosed that she is a member of the Board of Director n recommendations for the clinical practice guideline. Dr Haesler thank the other members of the nutrition work group: Merrilyn B (if any), in any position to control the content of this CME/CNE ac ies relevant to this educational activity.

st read the CME article and complete the quiz online, answering 8, 2022, and for nurses March 4, 2022. All tests are now online o information is on the last page of this article.

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INTRODUCTION Nutrition plays an important role in the prevention and treatment of pressure injuries (PIs). Macro- and micro- nutrients are required by each organ system in specific amounts to promote growth, development, maintenance, and repair of body tissues. The 2019 European Pressure Ul- cerAdvisory Panel (EPUAP), National Pressure Injury Advi- sory 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 orga- nizations. 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 profes- sionals around the world to use the recommendations generated to prevent and treat PI.

s for the National Pressure Injury Advisory Panel and the cochair of the small work group has disclosed that she is the consultant methodologist for the guideline on which this anks, Angela Liew, and Siriluck Sirlpanyawat. The authors, faculty, staff, and planners, tivity have disclosed that they have no financial relationships with, or financial interests

at least 14 of the 20 questions correctly. This continuing educational activity will expire nly; take the test at http://cme.lww.com for physicians and www.nursingcenter.com for

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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 con- text 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 implemen- tation considerations. Table 1 presents the nutrition-related recommendations from the EPUAP/NPIAP/PPPIA CPG, including the strengths of evidence and assigned

Table 1. 2019 INTERNATIONAL GUIDELINE NUTRITION RECOM The strength of evidence (SoE) ratings used in this table are defined as follows: B1, lev high or moderate quality providing directevidence, and/or most studies have consisten providing direct evidence, level 3 or 4 studies (regardless of quality) providing direct ev explained; C, level 5 studies (indirect evidence) and/or body of evidence with inconsist Statements (GPSs; statements that are not supported by a body of evidence but consid strength of recommendation (SoR) ratings are as follows: ↑↑, strong positive recomm

No.a Recommendation 1.10 Consider the impact of impaired nutritional status on the risk of pressu 4.1 Conduct nutritional screening for individuals at risk of a pressure injury 4.2 Conduct a comprehensive nutrition assessment for adults at risk of a p

malnutrition and for all adults with a pressure injury. 4.3 Develop and implement an individualized nutrition care plan for individ

malnourished or who are at risk of malnutrition. 4.4 Optimize energy intake for individuals at risk of pressure injuries who 4.5 Adjust protein intake for individuals at risk of pressure injuries who are 4.6 Provide 30 to 35 kcalories/kg body weight/day for adults with a pressu

malnutrition. 4.7 Provide 1.25 to 1.5 g protein/kg body weight/day for adults with a pre

malnutrition. 4.8 Offer high-calorie, high-protein fortified foods and/or nutritional supplem

at risk of developing a pressure injury and who are also malnourished cannot be achieved by normal dietary intake.

4.9 Offer high calorie, high protein nutritional supplements in addition to the malnourished or at risk of malnutrition, if nutritional requirements cann

4.10 Provide high-calorie, high-protein, arginine, zinc and antioxidant oral nu with a Category/Stage II or greater pressure injury who are malnourish

4.11 Discuss the benefits and harms of enteral or parenteral feeding to suppo care with individuals at risk of pressure injuries who cannot meet their nutritional interventions.

4.12 Discuss the benefits and harms of enteral or parenteral feeding to supp and goals of care for individuals with pressure injuries who cannot me despite nutritional interventions.

4.13 Provide and encourage adequate water/fluid intake for hydration for an i and clinical conditions.

4.14 Conduct age appropriate nutritional screening and assessment for neo 4.15 For neonates and children with or at risk of pressure injuries who have

appropriate nutritional supplements, or enteral or parenteral nutritional 22.2 Provide pressure injury education, skills training and psychosocial suppo aFor ease of reference, the recommendation number published in the Clinical Practice Guideline has bAs published in the Clinical Practice Guideline. Adapted with permission from the European Pressure Ulcer Advisory Panel, National Pressure Injury

ADVANCES IN SKIN & WOUND CARE • MARCH 2020 124

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recommendations. With the recommendations presented in Table 1 in mind, this article will discuss the underpin- ning research and the context in which the recommenda- tions 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

MENDATIONS el 1 studies of moderate or low quality providing direct evidence, level 2 studies of toutcomes and inconsistencies can be explained; B2, level 2 studies of low quality idence, and/or most studies have consistent outcomes and inconsistencies can be encies that cannot be explained, reflecting genuine uncertainty; and Good Practice ered by the Guideline Governance Group to be significant for clinical practice). The endation: definitely do it; ↑, weak positive recommendation: probably do it.

SoE, SoR, or GPSb

re injuries. SoE = C; SoR =↑ . SoE = B1; SoR =↑↑ ressure injury who are screened to be at risk of SoE = B2; SoR =↑↑

uals with, or at risk of, a pressure injury who are SoE = B2; SoR = ↑↑

are malnourished or at risk of malnutrition. SoE = B2; SoR = ↑ malnourished or at risk of malnutrition. GPS re injury who are malnourished or at risk of SoE = B1; SoR = ↑

ssure injury who are malnourished or at risk of SoE = B1; SoR =↑↑

ents in addition to the usual diet for adults who are or at risk of malnutrition, if nutritional requirements

SoE = C; SoR = ↑

usual diet for adults with a pressure injury who are ot be achieved by normal dietary intake.

SoE = B1; SoR = ↑↑

tritional supplements or enteral formula for adults ed or at risk of malnutrition.

SoE = B1; SoR = ↑

rt overall health in light of preferences and goals of nutritional requirements through oral intake despite

GPS

ort pressure injury treatment in light of preferences et their nutritional requirements through oral intake

SoE = B1; SoR = ↑

ndividual injury, when compatible with goals of care GPS

nates and children at risk of pressure injuries. GPS inadequate oral intake, consider fortified foods, age support.

GPS

rt to individuals with or at risk of pressure injuries. SoE = C; SoR = ↑

been used.

Advisory Panel, and Pan Pacific Pressure Injury Alliance.

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prognostic studies reporting multivariable analyses that in- cluded at least one measure of nutrition status, 40% identi- fied a measure of nutrition as a significant predictor of PIs. This suggests there is a moderate statistical association be- tween 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 pe- diatric PI risk factor studies to date; however, it is reason- able 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, in- cluding 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 regard- ing the significance of these outcome measures as posi- tive 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 nu- merous 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 num- ber of participants with extremely low or high weights/ BMIs in the sample. Translating research into clinical practice requires clin-

ical judgment informed by knowledge of the literature.1

When undertaking a PI risk assessment, the use of clini- cal judgment that considers the individual’s overall pre- sentation and the significance of that individual’s nutrition status is required. For example, if an individual presents with other risk factors considered highly pre- dictive of PI risk (eg, immobility), and the individual’s clinical condition is vulnerable, nutrition should be con- sidered 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 hos- pital were analyzed. From 16 factors included in the pre- dictive 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 nutri- tion (and other) care planning. WWW.ASWCJOURNAL.COM 125 Copyright © 2020 Wolters Kluwer Malnutrition Malnutrition involves several disorders that include under- nutrition, obesity, and abnormal micronutrient levels. Other nutrition-related disorders that impact an individual’s nutri- tion status include frailty, sarcopenia, and cachexia, which have multifaceted pathogenic origins.27 The European Soci- ety 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 Initia- tive on Malnutrition developed criteria to help identify malnutrition in adults in healthcare settings, consisting of three phenotype characteristics (weight loss, low BMI,de- creased muscle mass) and two etiologic characteristics (de- creased food intake or assimilation and disease burden/ inflammation). The presence of one phenotype and one etiologic characteristic is required.29 Table 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, in- sufficient nutrient intake and low body weight are both associated with impaired wound healing.5,30–35 International research suggests there is a relationship be- tween nutrition and PI prevalence. In the US, a study of 2,425 patients concluded that 76% of participants were mal- nourished.36 An Australian study conducted in acute and long-term care settings found that, for adults with malnutri- tion, the odds ratio of developing a PI was 2.6 (95% confi- dence 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 devel- opment 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 re- view, 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 ADVANCES IN SKIN & WOUND CARE • MARCH 2020 Health, Inc. All rights reserved. http://WWW.ASWCJOURNAL.COM Table 2. DIAGNOSTIC CHARACTERISTICS FOR MALNUTRITION Characteristic ASPEN/Academy of Nutrition and Dietetics ESPEN GLIM Unintended weight loss X X Low body mass index X X Loss of muscle mass X X Loss of subcutaneous fat X X Localized or generalized fluid accumulation X Decreased functional status X Reduced food intake or assimilation X X Disease burden/ inflammation X At risk per validated screening tool X Two of the six characteristics must be present Once the person is deemed at risk by a validated screening tool, one of the other two items must be present. One phenotype and one etiologic characteristic must be present Abbreviations: ASPEN, American Society for Parenteral and Enteral Nutrition; ESPEN, European Society for Parenteral and Enteral Nutrition; GLIM, Global Leadership Initiative on Malnutrition. Sources: White JV, Guenter P, Jensen G, et al. Consensus statement: Academy of Nutrition and Dietetics and American Society for Parenteral and Enteral Nutrition: characteristics recommended for the identification and documentation of adult malnutrition (undernutrition). J Parenter Enteral Nutr 2012;36(3):275-83. Cederholm T, Jensen GL, Correia MITD, et al.29 Undernutrition. Decreased intake of calories, protein, vitamins, and minerals is commonly seen in individuals with malnutrition, which is often associated with under- nutrition. 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 consid- ered a major risk factor for both malnutrition and PI development.41 Overnutrition/Obesity. Overnutrition is a form of mal- nutrition in which the amount of nutrients consumed ex- ceeds the amount of nutrients needed to support growth, ADVANCES IN SKIN & WOUND CARE • MARCH 2020 126 Copyright © 2020 Wolters Kluwer H 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 pro- portions. The CDC reported its prevalence was 39.8% in 2015 and 2016.43 Obesity has been linked to health condi- tions such as cardiovasculardisease, diabetes, cancer, hyper- tension, dyslipidemia, respiratory problems, and impaired wound healing.43 Comorbidities such as skin infection, dehiscence, PIs, and venous ulcers are common in obese individuals. These con- ditions occur because of hypoperfusion and ischemia in subcutaneous adipose tissue. Hypovascularity also contrib- utes to the prevalence of PIs in patients who are obese.44 The decreased mobility and difficulty with self-repositioning of- ten associated with individuals who are obese or extremely obese further increase the risk of PI development. Microor- ganisms that are attracted to the moist environment created by skin folds contribute to infections and tissue injuries.44 NUTRITION SCREENING This is defined as “the process of identifying patients, cli- ents, or groups who may have a nutrition diagnosis and benefit from nutrition assessment and intervention by a registered dietitian nutritionist.”45 Recognizing that nu- trition 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 ob- tained.47,48 Validated tools should be quick and easy to use, reliable and valid, economical, of low risk to the in- dividual being screened, and appropriate for the popu- lation and care setting. Nutrition screening and rescreening should be con- ducted 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 regula- tions. 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, WWW.ASWCJOURNAL.COM ealth, Inc. All rights reserved. http://WWW.ASWCJOURNAL.COM unintentional weight changes, changes in intake/appetite, lifestyle habits (physical activity, tobacco use), gastrointesti- nal 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 in- creased 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 identi- fication of impaired nutrition status allowed for the timely development and implementation of interventions.50 Fur- ther, a prospective cohort study of 471 patients admitted to a medical center in Helsinki concluded that decreased nu- trition 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 inter- mediate 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 neo- natal 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 WWW.ASWCJOURNAL.COM 127 Copyright © 2020 Wolters Kluwer Pediatric malnutrition leads to complex hospital stays because of the complications from underlying diseases and conditions such as slow wound healing. In these pa- tients, this contributes to increased hospital costs and length of stay.63 The ASPEN defines pediatric malnutri- tion (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 out- comes.”64 Many factors are involved in defining pediat- ric malnutrition including illness, injury, and adverse environmental or behavioral conditions. The Academy of Nutrition and Dietetics and ASPEN’s consensus state- ment on the indicators of pediatric malnutrition (undernu- trition) for ages 1 month to 18 years recommends that a standardized set of diagnostic indicators be used to iden- tify 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 da- tum is available.65 When two or more data points are avail- able, 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 compro- mised 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 com- promise their ability to consume adequate nutrients to promote and maintain wound healing.66 Early nutrition screening and assessment are important to identify mal- nutrition risk and implement a care plan. The EPUAP/ NPIAP/PPPIA CPG recommends providers conduct an age-appropriate nutritional screen and assessment for neo- nates and children at risk of PIs (Table 1).1 There are vari- ous 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. Anthropomet- ric data including weight, height, growth scores, head circumference, and Z scores are used to determine if a neonate or child is developing according to estab- lished 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 micro- nutrient deficiencies and signs of malnutrition. They should ADVANCES IN SKIN & WOUND CARE • MARCH 2020 Health, Inc. All rights reserved. http://WWW.ASWCJOURNAL.COM conduct weekly nutrition assessments for critically ill chil- dren.68–70 The healthcare team, including the RDN and pe- diatrician, should devise an individualized nutrition plan for the pediatric patients, and it should include the mode of feeding, frequent monitoring of intake and growth sta- tus, oral supplements, nutrition support, and feeding strat- egies for parents and caregivers.67,71 NUTRITION ASSESSMENT The EPUAP/NPIAP/PPPIA CPG recommends the com- pletion 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 interprofes- sional 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 ba- sic steps: nutrition assessment, diagnosis, interventions, and plan monitoring and evaluation. The nutrition assessment should be completed by an RDN in collaboration with the interprofessional nutri- tion 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, swallow- ing 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 de- scribed in the medical records as “well nourished.” Tak- ing 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 ADVANCES IN SKIN & WOUND CARE • MARCH 2020 128 Copyright © 2020 Wolters Kluwer H 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 malnu- trition. The recommendation for protein is 1.25 to 1.5 g/kg of body weight per day.1 Providing and consuming adequate kilocalories sup- port collagen and nitrogen synthesis, thus promoting anabolism by sparing protein from being used as an en- ergy source. Fat is the most concentrated source of calo- ries, 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 re- quirements. 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 in- take 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 opti- mized for the individual. This should be done within the context of the individual’s nutrition status (eg, cur- rent, usual, and goal weights) and clinical condition. The EPUAP/NPIAP/PPPIA CPG also provides spe- cific 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 calcu- lated using resting energy expenditure � activity factor 1.1 � stress factor 1.3 to 1.5 (mean intake, 37.9 ± 6.5 kcal/kg WWW.ASWCJOURNAL.COM ealth, Inc. All rights reserved. http://WWW.ASWCJOURNAL.COM 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 require- ments should be assessed frequently to avoid over or un- der 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 Protein is vital for the growth and maintenance of cells, fluid balance, and blood clotting; its functions include im- mune function preservation, wound healing enzyme re- pair and synthesis, cell multiplication, and collagen and connective tissue synthesis. Additional protein is also re- quired 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 re- ceiving higher-protein/higher-calorie diets had a statis- tically 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 com- pared with a low protein intake. An RCT by Lee et al82 reported that providing a standard diet with a concen- trated 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 heal- ing 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 deteriora- tion or no improvement in healing. Finally, in a trial by Ohura et al80 comparing the efficacy of two different nu- trition 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 im- proved 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 WWW.ASWCJOURNAL.COM 129 Copyright © 2020 Wolters Kluwer 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 Fluid/Water 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 sol- vent 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 pro- viders encourage adequate fluid intake. Although cur- rent 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 of- fered to and encouraged for all individuals with PIs. Those with draining wounds, emesis, diarrhea, elevated temperature, or increased perspiration require addi- tional 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 de- creasing the percentage of water their bodies can store. This, combined with a decreased sense of thirst, in- creases 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. Micronutrients 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 is- sue. Many of the oral supplements, enteral formulas, and for- tified 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, ap- proaches should be comprehensive, relying first on im- proving oral intake.89,90 Prior to or in addition to offering ADVANCES IN SKIN & WOUND CARE • MARCH 2020 Health, Inc. All rights reserved. http://WWW.ASWCJOURNAL.COM 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 bal- ance to sustain anabolism plays a crucial role in skin vi- ability 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 feed- ing 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 pos- itive 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, pro- viders 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 con- tribution 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 inci- dence 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 sub- stantiated 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 re- cent large double-blind RCT (the Oligo Element Sore ADVANCES IN SKIN & WOUND CARE • MARCH 2020 130 Copyright © 2020 Wolters Kluwer H Trial) has elucidated the independent role of these addi- tional 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 anti- oxidants 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 in- tervention 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 re- sponsible for a reduction in length of hospital stay when compared with usual care (standard diet).104–106 Analy- sis 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 con- trol formula.99 With this background, the use of ONSs in preventing and treating PIs could be recommended. NUTRITION SUPPORT Despite limited evidence supporting artificial nutrition and hydration for PI intervention and treatment, the inter- professional 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 inter- vention. The interdisciplinary team should consider if the patient has the desire and/or capacity to tolerate nu- trition 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 lim- ited impact on preventing PI for those at risk.94,95,107,108 The high-acuity level of patients in acute or long-term care in- creases 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 de- veloping 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 consis- tent with the individual’s goals of care. The RDN and interprofessional team should evaluate the patient’s WWW.ASWCJOURNAL.COM ealth, Inc. All rights reserved. http://WWW.ASWCJOURNAL.COM Table 3. NUTRIENTS AND THEIR THERAPEUTIC PROPERTIES Nutrient Functions Notes Sources Related CPG Recommendation Calories Supply energy, prevent weight loss, preserve lean body mass Carbohydrate, protein, and fat; carbohydrate and fat are preferred 4.6, 4.8, 4.9, 4.10 Carbohydrates Glucose supports cell growth, fibroblasts, and leukocytes Delivers energy; energy needs must be met to spare protein from being used for energy Grains, fruits, and vegetables; complex carbohydrates are preferred Protein Immune support; binding of skin, cartilage, and muscle Contains nitrogen, which is essential for wound healing. Arginine becomes a conditionally indispensable amino acid during times of physiologic stress Meats, fish, poultry, eggs, legumes, milk, and dairy products; favor lean meat and reduced- or low-fat dairy products 4.5-4.10 Fat Carries fat-soluble vitamins, provides insulation under the skin and padding of bony prominences, helps modulate inflammation and the immune response Most concentrated energy source Meats, eggs, dairy products, and vegetable oils Fluids/water Solvent for minerals and vitamins, amino acids, and glucose; helps maintain body temperature; transports materials to cells and waste products from cells; maintains skin integrity Water, juices, beverages; fruits and vegetables contain approximately 95% water. Most supplements are 75% water 4.13 Vitamin A Protein synthesis, collagen formation, maintenance of epithelium, immune function May delay healing in older adults on corticosteroids UL is 3,000 μg; DRI females aged >70 y is 700 μg, males aged >70 y is 900 μg

Beef liver, milk, dark green and yellow vegetables (carrots, sweet potatoes, broccoli, spinach, apricots)

Vitamin C Collagen formation, enhances activation of leukocytes and macrophages to wounds, improves tensile strength, aids in iron absorption

Water-soluble, noncaloric organic nutrient

Citrus fruits and juices, tomatoes, potatoes, broccoli

Vitamin E Fat metabolism, collagen synthesis, cell membrane stabilization

Antioxidant Vegetable oils, sweet potatoes

Copper Red blood cell formation, responsible for collagen cross-linking and erythropoiesis

Inorganic, noncaloric nutrient UL is 10,000 μg. DRI females and males aged ≥70 y is 900 μg.

Nuts, dried fruit, organ meats, dried beans, whole-grain cereal

Iron Transports oxygen to the cells as a component of hemoglobin, important in collagen formation, creates energy from cells

Heme iron: meats, poultry, and fish Nonheme iron: vegetables, grains, eggs, meat, fish

Zinc Cofactor for collagen formation, metabolizes protein, assists in immune function, liberates vitamin A from the liver, interacts with platelets in blood clotting

Inorganic, noncaloric nutrient Mega doses of zinc may inhibit healing and cause copper deficiency UL is 40 mg DRI females aged ≥70 y is 8 mg, males aged ≥70 y is 11 mg.

Meats, liver, eggs, and seafood

Abbreviations: CPG, EPUAP/NPIAP/PPPIA Clinical Practice Guideline; DRI, dietary reference intake; UL, tolerable upper intake level. Adapted with permission from Bernstein M, Munoz N. Nutrition for the Older Adult. 3rd ed. Burlington, MA: Jones and Bartlett Learning; 2020.

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 cul- tural and/or religious values may dictate their decision to accept or decline EN.

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If the gastrointestinal tract is functioning, EN is the pre- ferred 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

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age. These formulas meet the recommended dietary refer- ence 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 interpro- fessional team should frequently evaluate the patient’s toler- ance to EN and note any adverse reactions such as nausea, diarrhea, or vomiting. Cliniciansshould 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 re- lation to the desired outcome of healing and stabilizing nu- trition status in the medical record. They should also monitor and evaluate the individual’s tolerance and prog- ress toward achieving the desired outcome and recom- mended changes as needed. Research reviewing EN for improved outcomes for PI

healing is limited. Two high-level studies, one with 60 indi- viduals 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 Palliative Care/Hospice Patientsreceivingpalliativecareareathighriskofdeveloping 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 fam- ilies and/or caregivers (Table 1). The guiding principles of palliative care for PI man- agement focus on relieving pain and providing comfort for the individual. Nutrition interventions should be com- patible with patient goals and desired outcomes. For exam- ple, 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 Di- etetics that “individuals have the right to request or re- fuse 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 individualizednutrition care plan be developed. The interdisciplinary team is responsible for ADVANCES IN SKIN & WOUND CARE • MARCH 2020 132 Copyright © 2020 Wolters Kluwer H nutrition care that addresses the desired outcomes for the in- dividual. 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 im- proved wound healing compared with standardized nutri- tion plans (37% vs 23.4%, P < .05). The care plan process should encompass the policies and/or regulations of the or- ganization. The RDN builds the nutrition care plan based on the information gathered in the nutrition assessment, in- cluding data generated by the physician; nurses; and phys- ical, 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 • educatetheindividual/caregiveronthebenefitsofthesuggested 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 in- clude 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 pa- tients with literacy or language difficulties. Some US hospitals host a Food Pharmacy including ONSs for in- dividuals who have limited access to affordable and nu- tritious foods. Wound care clinics and rehabilitation departments, acute care hospitals, and post-acute care facilities are encouraged to provide hot and cold bever- ages 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 con- ditions and when progress toward the desired outcome is not achieved. The RDN may need to reassess the pa- tient or refer them to another discipline for further eval- uation 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 WWW.ASWCJOURNAL.COM ealth, Inc. All rights reserved. http://WWW.ASWCJOURNAL.COM Figure 1. GUIDE FOR THE NUTRITION MANAGEMENT OF PRESSURE INJURIES (PIS) FOR ADULTS IN ACUTE OR LONG-TERM CARE 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 sup- port programs can produce short-term positive impacts on knowledge, education, and quality of life.116–119 Pa- tients themselves have noted the importance of engag- ing 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 im- portant or very important in caring for themselves. Further, the survey respondents identified that nutrition educa- tion 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 in- formation 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) WWW.ASWCJOURNAL.COM 133 Copyright © 2020 Wolters Kluwer 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 pre- vention 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 popu- lation, the researchers noted that the willingness of indi- viduals to engage in education interventions is limited by their clinical condition.123 This suggests that appropri- ate timingis an important consideration for nutrition- related education. RESEARCH PRIORITIES Nutrition plays a vital role in human growth and devel- opment; the maintenance of good health and functional- ity; prevention and treatment of infectious, acute, and chronic diseases; and PI development and treatment. To effectively and efficiently advance the role of nutri- tion in improving and sustaining health and tissue via- bility 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 ADVANCES IN SKIN & WOUND CARE • MARCH 2020 Health, Inc. All rights reserved. http://WWW.ASWCJOURNAL.COM among patients at risk of or with PIs in all care settings. Key research priorities on nutrition and PI prevention and treat- ment 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, med- ical, social, and health history, also influences PI develop- ment. 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 nu- trition interventions in patients with PIs must always be considered among the outcomes of interest. CONCLUSIONS 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 var- iation and achieve positive outcomes. PRACTICE PEARLS • 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 in- dividualized 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.• REFERENCES 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. 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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 of nutrition 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 and assessment: 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: WWW.ASWCJOURNAL.COM 135 Copyright © 2020 Wolters Kluwer 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. 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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 2010;26(9): 867-72. 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. 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All rights reserved. http://www.eatrightpro.org/-/media/eatrightpro-files/practice/scope-standards-of-practice/20190910-academy-definition-of-terms-list.pdf http://www.eatrightpro.org/-/media/eatrightpro-files/practice/scope-standards-of-practice/20190910-academy-definition-of-terms-list.pdf http://www.nutritioncaremanual.org http://www.aci.health.nsw.gov.au/__data/assets/pdf_file/0004/388237/13.-Trans-Tasman-Dietetic-Wound-Care-Group-Pressure-Injury-Guidelines-2011.pdf http://www.aci.health.nsw.gov.au/__data/assets/pdf_file/0004/388237/13.-Trans-Tasman-Dietetic-Wound-Care-Group-Pressure-Injury-Guidelines-2011.pdf http://www.aci.health.nsw.gov.au/__data/assets/pdf_file/0004/388237/13.-Trans-Tasman-Dietetic-Wound-Care-Group-Pressure-Injury-Guidelines-2011.pdf http://www.ncpro.org http://www.ncpro.org http://WWW.ASWCJOURNAL.COM 111. Malone A, Carney IN, Mays A, eds. ASPEN Enteral Nutrition Handbook. 2nd ed. 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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. ADVANCES IN SKIN & WOUND CARE • MARCH 2020 136 Copyright © 2020 Wolters Kluwer H 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. For more than 150 additional continuing education articles related to Skin and Wound Care topics, go to NursingCenter.com/CE. CONTINUING MEDICAL EDUCATION INFORMATION FOR PHYSICIANS Lippincott Continuing Medical Education Institute, Inc., is accredited by the Accreditation Council for Continuing Medical Education to provide continuing medical education for physicians. Lippincott Continuing Medical Education Institute, Inc., designates this journal-based CME activity for a maximum of 1 AMA PRA Category 1 CreditTM. Physicians should claim only the credit commensurate with the extent of their participation in the activity. PROVIDER ACCREDITATION INFORMATION FOR NURSES Lippincott Professional Development will award 2.0 contact hours for this continuing nursing education activity. LPD is accredited as a provider of continuing nursing education by the American Nurses Credentialing Center's Commission on Accreditation. This activity is also provider approved by the California Board of Registered Nursing, Provider Number CEP 11749 for 2.0 contact hours. LWW is also an approved provider by the District of Columbia, Georgia, and Florida CE Broker #50-1223. OTHER HEALTH PROFESSIONALS This activity provides ANCC credit for nurses and AMA PRA Category 1 CreditTM for MDs and DOs only. All other healthcare professionals participating in this activity will receive a certificate of participation that may be useful to your individual profession's CE requirements. CONTINUING EDUCATION INSTRUCTIONS � Read the article beginning on page 123. For nurses who wish to take the test for CNE contact hours, visit http://nursing.ceconnection.com. For physicians who wish to take the test for CME credit, visit http://cme.lww.com. Under the Journal option, select Advances in Skin and Wound Care and click on the title of the CE activity. � You will need to register your personal CE Planner account before taking online tests. Your planner will keep track of all your Lippincott Professional Development online CE activities for you. � There is only one correct answer for each question. A passing score for this test is 14 correct answers. If you pass, you can print your certificate of earned contact hours or credit and access the answer key. Nurses who fail have the option of taking the test again at no additional cost. Only the first entry sent by physicians will be accepted for credit. Registration Deadline: February 28, 2022 (physicians); March 4, 2022 (nurses). PAYMENT �The registration fee for this CE activity is $17.95 for nurses; $22.00 for physicians. WWW.ASWCJOURNAL.COM ealth, Inc. All rights reserved. http://NursingCenter.com/CE http://http://nursing.ceconnection.com http://http://cme.lww.com http://WWW.ASWCJOURNAL.COM