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Protein Requirements in Illness: Considerations for Acute Care Nurse Practitioners
ORIGINAL RESEARCH
Protein Requirements in Illness: Considerations for Acute Care Nurse Practitioners
Shannon McMahon, MS, RD, LD, Linda Knol, PhD, RD, LD, Alice L. March, PhD, FNP, CNE, Jodie Bilbrey, MS, RD, Sarah L. Morgan, MD, RD, FADA, FACP, and Jeannine Lawrence, PhD, RD, LD ABSTRACT
This retrospective chart review (N ¼ 150) examined weight, height, urinary urea nitrogen, and feeding method in acutely ill adults. Using 2 evidence-based approaches, estimated protein needs were compared with laboratory-measured protein requirements. Comparisons were significantly associated for normal weight patients (r ¼ 0.21, P ¼ .03) but not for patients who were obese (r ¼ 0.10, P ¼ .49), showing that the use of body weight and standard formulas to calculate protein needs may not be appropriate for individuals who are obese. Considerations for individual patients should be considered. More research is needed to determine how to accurately estimate protein during acute illness in patients who are obese. Keywords: acutely ill adults, obesity, protein needs, urinary urea nitrogen Ó 2016 Elsevier, Inc. All rights reserved.
N
urse practitioners (NPs) in acute care settings are charged with providing safe and holistic care to increasingly complex patients. One facet of care is that NPs must have a working understanding of the nutritional needs of the acutely ill patient. In particular, the NP must understand protein needs, how those needs vary by body weight, and how protein usage is affected by acute illness. Even though the acute care NP may work in an interprofessional team with registered dietitians, the primary responsibility for the coordination of that care often falls to the NP. The application of standardized, disease-based protein recommendations to any acutely ill patient is problematic but is even more difficult in patients who are obese (body mass index [BMI] 30.0). Obesity is a disease state,1 which brings with it a chronic inflammatory process, increasing the need for adequate protein.2 Thus, there is a need to know if acutely ill patients who are obese have different protein needs when compared with those of normal weight. In addition, people who are obese may have comorbid conditions that warrant additional www.npjournal.org
considerations in the assessment and determination of protein needs. The obesity epidemic has challenged NPs to reassess old approaches to care and generate new standards of practice for patients who are obese. Improving clinical practice requires the use of evidence-based guidelines. Protein requirements in obesity and illness are not yet clearly established and are not well understood. Urinary urea nitrogen (UUN) can be used to estimate protein use during an acute illness, along with certain formulas designed to adjust for body weight. Thus, measuring UUN in people of differing body types (normal weight and obesity) may help to establish guidelines for estimating these needs. This retrospective chart review demonstrates an urgent need to examine how protein requirements for people who are obese could best be predicted. RESEARCH QUESTIONS
There are 2 research questions to consider. First, what is the relationship between body weight and dietary protein needs in acutely ill patients, as measured by a The Journal for Nurse Practitioners - JNP
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24-hour UUN test? Second, what is the relationship between measured protein needs and estimated protein needs in acutely ill patients who are obese? REVIEW OF THE LITERATURE
Protein is a vital macronutrient necessary for energy metabolism, digestion, blood clotting, vision, antibody formation, acid-base balance, and fluid regulation. It is also a key ingredient for growth, repair, and replacement of tissue.3 In times of illness and stress, adequate protein intake (or supplementation) can decrease the rate of muscle loss, improve immune function, and support recovery.4 Protein needs are associated with body composition, particularly obesity. An increase in adipose tissue results in a significant increase in body fat and a slight increase in lean body mass, which may affect these metabolic processes. Protein requirements for supporting health and promoting healing during an acute illness are well established for normal weight individuals5 (BMI, 18.5-24.9), yet there is a dearth of literature regarding protein requirements for obese patients (BMI 30.0).6,7 The first nitrogen balance studies, conducted as early as 1907, typically used small groups of healthy males who were of normal weight to determine the required protein needs to support general good health but not ill health.8,9 Nitrogen balance studies were then tailored for actual patient use in subsequent clinical studies that focused on specific disease states, thus generating protein recommendations (in g/kg) based on the patient diagnosis but not body weight.10,11 Protein needs are typically obtained in 1 of 2 ways. Measured needs are derived from laboratory tests. In the absence of measured needs, protein needs can be estimated using established calculations that incorporate factors such as height, weight, and injury. Currently, the most common laboratory test used to measure nitrogen balance in the clinical setting is a 24-hour UUN test.12 The UUN is a quick, simple, and inexpensive way to measure the catabolism of lean tissue and is the commonly accepted method of estimating nitrogen balance in clinical care patients.12-14 A 24-hour UUN test measures only the urea excreted in the urine; therefore, a standard formula has been developed to calculate protein loss from all sources using the results of the 24-hour 2
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UUN test with the addition of 4 g protein. This accounts for the loss of urea through feces, sweat, hair, skin, nails, creatinine, uric acid, and ammonia.15 In healthy subjects, UUN accounts for about 80% to 90% of urinary nitrogen losses, but illness stressors alter the production of urea and the results of the UUN test. Depending on the disease and type of stress, the amount of urinary urea accounted for by UUN can vary widely, falling well below or above the average.14 The urine collection technique and metabolic factors also affect the accuracy of 24-hour UUN results. For example, spills and leaking catheters result in inaccurate samples, and conditions such as edema, dialysis, renal insufficiency, and gastrointestinal bleeding alter test results.12,16 It is possible that a shorter collection period (6-12 hours) would help address some of these concerns.12 Despite the possible variances in UUN results, the test can still be used in conjunction with other assessment tools to monitor protein status and determine the best course of nutritional treatment for the patient.14 Current, well-developed protein guidelines specifically targeting acutely ill patients who are obese are lacking. Additionally, even fewer researchsupported recommendations for protein provision exist for critically ill patients who are obese and who may be receiving intentional hypocaloric feeding protocols. Guidelines suggest protein replacement of 2.0 g/kg ideal body weight (IBW) for patients with a BMI of 30.0 to 39.9 kg/m2 and 2.5 g/kg IBW for those with a BMI > 40.0 kg/m2.17 However, it is common practice to calculate a body weight adjustment in lieu of the patient’s actual body weight to estimate protein needs.6 The approaches include the use of IBW or adjusted body weight (ABW). The development and validation of body weight adjustment factors are not well documented. Data used to evaluate energy requirements are the basis for these body weight adjustment factors, yet little research supports their use in the determination of protein needs of patients who are obese.18,19 A common method for adjusting body weight in the United States is to calculate IBW using the Hamwi formula (males ¼ 106 pounds for the first 60 inches þ 6 pounds for every inch greater than 60 inches; females ¼ 100 pounds for the first 60 inches þ 5 pounds for every inch greater than 60 inches).18 Volume
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It is not clear how the formula was originally derived or whether it was ever well validated.18,19 The calculation of IBW uses only height and sex and does not account for an increase in fat-free mass (FFM). FFM is body mass comprised of approximately 75% water and 25% protein.20 ABW formulas, such as the Amato formula ([actual weight e IBW] 0.5 þ IBW), use IBW to calculate the protein needs to support FFM and then add an additional percent, typically 25% or 50% of the IBW, to account for the portion of metabolically active fat mass (fat in the adipose tissue).19,21 The purported intent of using ABW to estimate energy and protein needs in patients who are obese is to support the FFM, as well as a portion of the fat mass that is metabolically active.20,21 The original ABW formula first appeared in 1984, and it is uncertain how the formula for ABW was developed or if it is well validated.19,21 The Harris Benedict (HB) equation has been evaluated in obese populations, yet there remains a dearth of research about adjustment factors and estimated protein needs in patients who are obese. Two studies helped to establish the usefulness of the HB equation. In 1 study of women with normal and obese BMIs, the use of the HB equation combined with the actual body weight estimated energy needs with a 68% rate of accuracy. The underestimation of energy needs was 9%.22 When IBW was incorporated into the HB equation in lieu of the actual body weight, the opposite was found; energy needs were predicted accurately in 23% of cases, whereas energy needs were underestimated in 74% of the study participants. This shows the importance of the consideration of FFM. A similar study evaluated the precision of estimating energy needs in people who were obese using the HB equation with actual body weight versus using ABW (with adjustment factors of 25%).23 The results showed that energy needs were consistently underestimated when predicted by ABW in conjunction with the HB equation, and as BMI increased, the level of error in estimated needs also increased. When ABW (with adjustment factor) was used, there was a mean difference of 25% between measured and estimated energy needs in people who were obese. Additionally, in people with a BMI > 40.0 kg/m2, energy needs www.npjournal.org
were underestimated 100% of the time. When using actual body weight in the HB equation to calculate energy needs of people who were obese, the error rate was only 36%. In support of these findings, another group of researchers found the measured resting energy expenditure was significantly higher than the need estimated by the HB equation when IBW was included in the calculation.24 In summary, there appears to be a need for research that examines whether the estimation of protein needs in people who are obese should be based on actual body weight, IBW, or ABW. Therefore, the objectives of this study were to 1) investigate the relationship between body weight and dietary protein needs in acutely ill patients as measured by a 24-hour UUN test and 2) evaluate the relationship between measured protein needs and estimated protein needs in patients who were obese (using body weight adjustment factors in the predictive equations in lieu of actual body weight). METHODS
This study was a retrospective chart review of adult inpatients at a large facility in the Southeastern US. The study protocol received approval from the Institutional Review Boards for Human Subjects. Considering the variables in questions, a power analysis for a 2-sided hypothesis test with a significance level of 0.05 revealed that 150 charts were needed to achieve a power of 94%. A preliminary review of electronic medical records of patients on whom a UUN test had been collected during a single admission yielded a convenience sample of approximately 200 patients who fit the basic criteria. Considering the power analysis, number of charts available, and the reality that 25% of charts might be unusable because of study exclusion criteria, the goal for the sample size was set at 150 charts. Data collected from charts of 150 unique patients included age, sex, race, weight, height, a single UUN test result (as grams of nitrogen excreted) per admission, unit location at the time of UUN collection, feeding method, comorbidities, and admitting diagnosis. Weight at the time of admission and weight closest to the time of UUN collection were assessed, but only the weight closest to the UNN test was used for the calculation of body weight. The Journal for Nurse Practitioners - JNP
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The standard operating procedure at the facility was for daily weights to be taken on acute care units. Weights were taken using a bed scale and recorded in the medical record. The weight nearest the time of UUN collection was the weight used for analysis because a 24-hour UUN test was not always conducted on admission. Because this was a retrospective chart review, there was no way to determine the patients’ dry weight. The standard operating procedure for a 24-hour UUN test was to collect the urine sample in a 2-L container kept on ice in the patient’s room during the collection period. The start date and time and end date and time of the collection period were recorded in the medical record. Subjects were excluded if they were younger than 19 or older than 85 years of age, received hemodialysis at the time of UUN collection, had an insufficient urine volume (< 1.0 L) for UUN analysis, or were diagnosed with a gastrointestinal bleed or hepatic encephalopathy. For comparison of measured protein needs versus estimated protein requirements in patients who were obese, the IBW was calculated using the Hamwi formula, and ABW was calculated using the Amato formula.21 Subject charts were also coded with the BMI categories of normal weight, overweight, and obese as established by the World Health Organization.7 The majority (85.4%) of patients who were obese were within the BMI range of 30.0 and 39.9, and estimated protein requirements were calculated based on the recommendation of 2.0 g/kg for acutely ill patients who were obese (BMI ¼ 30.0-40.0 kg/m2) receiving hypocaloric feeding protocols.17 The results of the 24-hour UUN test were converted into grams of protein using the standardized formula ([24-hour UUN (g) þ 4 g] 6.25). Measured protein requirements determined from the results of UUN were then divided by actual weight, IBW, and ABW to generate a comparison of grams of protein per kilogram. Data Analysis
Descriptive characteristics (mean and standard deviation) were determined for the study population. Correlational analysis was used to evaluate the relationship of measured body weight with protein needs. There were 3 distinct outliers in the data set; 4
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therefore, the data analyses were run first with all subjects (N ¼ 150) and then subsequently without the 3 outliers. All subjects were included in the final analysis because the outcomes were the same for both analyses. Additional calculations estimated the precision (distance between the upper and lower confidence limits) of the 95% confidence interval for the Spearman rank correlation. This analysis showed a confidence interval width of 0.30. Paired Student t test and Spearman correlations assessed the relationship between estimated protein requirements using IBW, ABW, and measured protein requirements (UUN) in patients who were obese. Bland-Altman analyses graphically depicted agreement between protein requirements using IBW, ABW, and UUN in patients who were obese.25 All statistical tests were 2 tailed and performed using a significance level of < 0.05 using SAS (version 9.2, 2008; SAS Institute, Inc, Cary, NC). RESULTS
One hundred fifty subjects were included in the analyses, and the descriptive characteristics of the population are summarized in the Table. The study population was primarily comprised of white men, who were not of Hispanic or Latino ethnicity and ranged in age from 25 to 82 years of age (mean ¼ 61.9 10 years). Most subjects were between the ages of 50 and 69 and during admission were located in an intensive care unit at the time of the 24-hour UUN collection. Sources of nutrition at the time of specimen collection included parenteral nutrition, enteral nutrition, oral diet, or a combination of modalities. The number of patients who were not eating or receiving nutritional support included 2 underweight (BMI < 18.5), 4 normal weight (BMI ¼ 18.5-24.9), 4 overweight (BMI ¼ 25.0-29.9), and 3 obese (BMI ¼ 30.0-34.9) subjects. For the total group, the mean weight was 88.7 kg 26.9 kg, and the mean BMI was 26.9 7.7 kg/m2. The mean grams of protein excreted (UUN) was 95.6 35.4 g. Body weight was significantly associated with measured protein needs in the total group (r ¼ 0.29, P ¼ .0003) and in patients who were not obese (n ¼ 102, r ¼ 0.21, P ¼ .03; Figure 1). In patients who were obese, the measured protein needs were neither significantly associated with actual Volume
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Table. Demographic Data Variable
n
% Total
Range
Mean SD
Race White
82
54.7
Black or African American
62
41.3
Unknown
3
2.0
American Indian or Alaskan Native
2
1.3
Native Hawaiian or other Pacific Islander
1
0.7%
Sex Male Female
145
96.7
5
3.3
Age (years)
25-82
30
2
1.3
40-49
11
7.3
50-59
46
30.7
60-69
54
36.0
70-79
34
22.7
80
3
2.0
BMI
150
14.5-60.6
Underweight
20
13.3
14.5-18.49
Normal weight
47
31.3
18.5-24.9
Overweight
35
23.3
25.0-29.9
Obese
48
32.0
30.0-60.6
PO (per os)
23
15.3
TF
40
26.6
TPN
67
44.6
PO and TF
1
0.7
PO and TPN
1
0.7
TF and TPN
5
3.3
13
8.7
61.95 10.08
26.9 7.7
Feeding method
No nutrition support Weight (kg) used for 24-hour UUN
150
41.3-202.0
88.7 26.9
24-hour UUN results (grams of protein)
150
35.7-198.8
95.6 35.4
Underweight
20
41.2-184.3
92.0 40.1
Normal weight
47
38.1-182.0
85.8 30.4
Overweight
35
35.6-185.0
96.2 34.9
Obese
48
50.0-198.7
106.1 36.4
BMI ¼ body mass index; PO ¼ by mouth; SD ¼ standard deviation; TF ¼ tube feed; TPN ¼ total parenteral nutrition; UNN ¼ urinary urea nitrogen.
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Figure 1. Protein requirements as measured by urinary urea nitrogen excretion. 200
Protein (g)
150
100
Nonobese protein
50
Obese Linear (Nonobese protein) 0 25
45
65
85
105
125
145
165
185
205
225
Body weight (kg)
body weight (n ¼ 48, r ¼ 0.10, P ¼ .49; Figure 1), nor with estimated body weight using the body weight adjustment factors of IBW (r ¼ 0.02, P ¼ .86) or ABW (r ¼ 0.08, P ¼ .56). In the group of patients who were obese, the measured protein needs were 0.95 g/kg ( 0.38) of actual body weight. The predicted protein needs using IBW multiplied by 2.0 g/kg were higher and averaged 1.45 g/kg ( 0.52). The ABW multiplied by 2.0 g protein/kg was also higher and averaged 1.14 g/kg ( 0.42). Measured protein needs were significantly different from the protein needs predicted using IBW and ABW (P ¼ .001 for each), and the estimated protein needs typically overpredicted protein requirements (Figure 2). The use of IBW or ABW multiplied by 2.0 g protein/kg to predict protein requirements accurately predicted protein needs (within 10% of measured protein use) in 14.6% (n ¼ 7) and 8.3% (n ¼ 4; IBW and ABW, respectively) of the acutely
ill patients who were obese. Body weight adjustment factors used to predict protein requirements actually overpredicted (by > 110% of measured protein needs) in the majority of acutely ill patients who were obese. This overprediction occurred in 72.9% (n ¼ 35) when using IBW, 89.6% (n ¼ 43) when using ABW adjustments, and by 62.8 ( 24.9) and 93.8 ( 38.7) g protein when using the IBW and ABW, respectively. The error may occur because obesity represents a disproportionate ratio of leanto-fat mass, a criterion not present in the body weight adjustment calculation; thus, the use of those factors may represent incorrect assumptions about actual body composition in people who are obese.19 RECOMMENDATIONS
This study has implications for NPs, as well as other advanced practice nurses. The study shows that there is a need to consider how patients’ protein needs during acute illness are affected by body weight but may not be generalizable to well patients living in the community. For NPs providing care to acutely ill patients, these findings suggest that estimated protein needs based on either IBW or ABW are significantly different from the actual protein requirements of acutely ill patients who were obese. Interestingly, protein needs are typically greatly overestimated for this population. Because of the growing obesity epidemic, there is an urgent need to develop evidence-based guidelines specific to protein replacement in this population. Armed with this information, the NP helps provide consistency in
Figure 2. Bland-Altman plots.
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the standard of care and can engage the interprofessional team in meaningful discussions about dietary replacement of protein during acute illness. The objectives of this study were 2-fold. The primary objective was to investigate the relationship between BMI and measured protein needs (by 24-hour UUN) to determine if body weight was significantly associated with measured protein needs. A significant association between body weight and measured protein needs was observed for the entire group and in patients who were not obese but not the subset of patients who were obese. It is possible that the association between body weight and measured protein needs observed in the total group was driven by patients with normal BMIs. However, the study did suggest that the use of IBW and ABW calculation methods may be adequate for acutely ill adults who are not obese. This is an important consideration for acute care NPs working in interprofessional teams who are ordering nutritional support for acutely ill patients. The secondary study objective was to investigate the relationship between measured protein needs and estimated protein needs in patients who were obese by utilizing the IBW and ABW calculations commonly used in clinical practice. This study was unique in its assessment of the adequacy of estimation of protein needs based on predictive equations using IBW and ABW for patients who were obese. In examining the relationship between measured protein needs and adjusted body weight (IBW or ABW), this study found that measured protein needs were not associated with body weight in patients who were obese, even after using standard body weight adjustment factors. Additionally, we found that protein requirements as estimated by either IBW or ABW were significantly higher than measured protein needs (P < .001 for each). This study did have limitations. Similar to early nitrogen balance studies, our study population was comprised of a high percent of men, with charts of only 5 women available. Fluid imbalance alters both body weight and the relationship between measured and predicted protein needs, and the use of a retrospective chart review precluded the ability to assess patients for fluid overload. These factors may be seen as flaws to the design and may have www.npjournal.org
affected outcomes. To adjust for the unmet assumption of a normal distribution, Spearman correlations were used. One potential limitation may actually be a benefit of this study. Although most nitrogen balance studies focus on determining protein needs for patients with a particular disease state or at least stratify by disease state, this study did neither. Although not stratifying by disease state may have contributed to the variability in measured protein needs, the examination of results by BMI category lends strength to the study because it provides a more accurate representation of clinical practice and may, therefore, be more applicable across a range of disease states. To further explore the relationship between body weight and protein needs and to ensure that actual protein needs of acutely ill patients who are obese are being met, future research needs to be conducted. To offset the increased risk of error from a 24-hour UUN collection period, it has been suggested that a 6- or 12-hour collection period may be more effective.12 Studies should be prospective in nature and should control for caloric and fluid intake in addition to measuring protein excretion. The study population should be expanded to allow for the examination of various levels of protein provision, instead of 1 set provision rate; include an equal proportion of male and female subjects and ethnically diverse populations; and ensure all BMI categories are fully represented. CONCLUSIONS
The findings from previous studies22-24 and the current study support the position that using body weight adjustment factors to estimate nutritional needs may not correctly predict the true needs of patients. This study suggests that protein needs are directly associated with body weight in acutely ill patients with normal BMIs but that the same association is not seen for acutely ill patients who are obese. Additionally, protein needs calculated using adjustment factors such as IBW or ABW resulted in estimated needs that were not correlated with and were overestimates of measured needs. Acute care NPs should use interprofessional teams and, in particular, should seek the advice and The Journal for Nurse Practitioners - JNP
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expertise of the registered dietician on the team. When measurement of protein excretion to better determine actual protein requirements is unavailable, there may not be a clear advantage to using ABWs in estimating protein needs in the acutely ill patient who is obese. References 1. AMA. American Medical Association House of Delegates. Recognition of Obesity as a Disease. Resolution pp. 2. http://media.npr.org/documents/2013/ jun/ama-resolution-obesity.pdf. 2013. Accessed June 20, 2015. 2. Port AM, Apovian C. Metabolic support of the obese intensive care unit patient: a current perspective. Curr Opin Clin Nutr Metab Care. 2010;13:184-191. 3. Whitney E, Rolfes SR. Protein: amino acids. In: Adams P, ed. Understanding Nutrition. 11th ed. Belmont, CA: Thomas Wadsworth; 2008:180-203. 4. Winkler MF, Malone AM. Medical nutrition therapy for metabolic stress: sepsis, trauma, burns, and surgery. In: Mahan LK, Escott-Stump S, eds. Krause’s Food and Nutrition Therapy. 12th ed. Philadelphia, PA: Saunders Elsevier; 2008:1021-1041. 5. Institute of Medicine of the National Academies. Dietary Reference Intakes for Energy, Carbohydrates, Fiber, Fat, Protein, and Amino Acids (Macronutrients). Washington, DC: The National Academies Press; 2002/2005. 6. Ventura JM. Protein requirements and losses: surgical wounds and drains. Support Line. 2008;30:8-13. 7. Physical Status: The Use and Interpretation of Anthropometry. Report of a WHO Expert Committee (Technical Report Series No. 854). Geneva: World Health Organization; 1995:329. 8. Energy and Protein Requirements. Report of a Joint FAO/WHO Ad Hoc Expert Committee (Technical Report Series No. 522). Geneva: World Health Organization; 1973. 9. Bodwell CE, Schuster EM, Kyle E, et al. Obligatory urinary and fecal nitrogen losses in young women, older men, and young men and the factorial estimation of adult human protein requirements. Am J Clin Nutr. 1979;32:2450-2459. 10. Ishibashi N, Plank LD, Sando K, Hill G. Optimal protein requirements during the first 2 weeks after the onset of critical illness. Crit Care Med. 1998;26:1529-2459. 11. Swart GR, van den Berg JWO, van Vuure JK, Rietveld T, Wattimena DL, Frenkel M. Minimum protein requirements in liver cirrhosis determined by nitrogen balance measurements at three levels of protein intake. Clin Nutr. 1989;8:329-336. 12. Graves C, Saffle J, Morris S. Comparison of urine urea nitrogen collection times in critically ill patients. Nutr Clin Pract. 2005;20:271-275. 13. Bingham SA. Urine nitrogen as a biomarker for the validation of dietary protein intake. J Nutr. 2003;133:921S-924S. 14. Konstantidines FN. Nitrogen balance studies in clinical nutrition. Nutr Clin Pract. 1992;7:231-238. 15. Gropper SS, Smith JL, Groff JL. Protein. In: Gropper SS, Smith JL, Groff JL, eds. Advance Nutrition and Human Metabolism. 5th ed. Belmont, CA: Wadsworth CENGAGE Learning; 2009:179-250. 16. Heimburger DC. Nutrition Assessment. In: Heimburger DC, Ard JD, eds. Handbook of Clinical Nutrition. 4th ed. Philadelphia, PA: Mosby Elsevier; 2006:242-261. 17. Choban P, Dickerson R, Malone A, Worthington P, Compher C. American Society for Parenteral and Enteral Nutrition. A.S.P.E.N. Clinical guidelines: nutrition support of hospitalized adult patients with obesity. JPEN J Parenter Enteral Nutr. 2013;37:714-744.
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18. Shah B, Sucher K, Hollenbeck CB. Comparison of ideal body weight equations and published height-weight tables with body mass index tables for healthy adults in the United States. Nutr Clin Pract. 2006;21: 312-319. 19. Ireton-Jones C. Adjusted body weight, con: why adjust body weight in energy-expenditure calculations? Nutr Clin Pract. 2005;20:474-479. 20. Choban PS, Dickerson RN. Morbid obesity and nutrition support: is bigger different? Nutr Clin Pract. 2005;20:480-487. 21. Krenitsky J. Adjusted body weight, pro: evidence to support the use of adjusted body weight in calculation calorie requirements. Nutr Clin Pract. 2005;20:468-473. 22. Weijs PJM, Vansant GAAM. Validity of predictive equations for resting energy expenditure in Belgian normal weight to morbid obese women. Clin Nutr. 2010;29:347-351. 23. Frankenfield DC, Rowe WA, Smith JS, Cooney RN. Validation of several established equations for resting metabolic rate in obese and nonobese people. J Am Diet Assoc. 2003;103:1152-1159. 24. Feurer ID, Crosby LO, Buzby GP, Rosato EF, Mullen JL. Resting energy expenditure in morbid obesity. Ann Surg. 1983;197:17-21. 25. Bland JM, Altman DG. Measuring agreement in method comparison studies. Stat Methods Med Res. 1999;8:135-160.
Shannon McMahon, MS, RD, LD, is an instructor with the Department of Human Nutrition and Hospitality Management at The University of Alabama in Tuscaloosa. Linda Knol, PhD, RD, LD, is an associate professor at The University of Alabama. Alice L. March, PhD, FNP, CNE, is an assistant dean of graduate programs and associate professor with Capstone College of Nursing at The University of Alabama and can be reached at [email protected]. Jodie Bilbrey, MS, RD, is a retired clinical dietitian with the Department of Nutrition and Foodservices at the Veterans Department of Affairs Medical Center in Birmingham, AL. Sarah L. Morgan, MD, RD, FADA, FACP, is a professor of medicine and nutrition sciences and medical director at the UAB Osteoporosis Prevention and Treatment Clinic and Bone Densitometry Service in Birmingham, AL. Jeannine Lawrence, PhD, RD, LD, is an associate professor with the Department of Human Nutrition and Hospitality Management at the University of Alabama. In compliance with national ethical guidelines, the authors report no relationships with business or industry that would pose a conflict of interest. 1555-4155/16/$ see front matter © 2016 Elsevier, Inc. All rights reserved. http://dx.doi.org/10.1016/j.nurpra.2016.03.010
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Protein Requirements in Illness: Considerations for Acute Care Nurse Practitioners
Shannon McMahon, MS, RD, LD, Linda Knol, PhD, RD, LD, Alice L. March, PhD, FNP, CNE, Jodie Bilbrey, MS, RD, Sarah L. Morgan, MD, RD, FADA, FACP, and Jeannine Lawrence, PhD, RD, LD ABSTRACT
This retrospective chart review (N ¼ 150) examined weight, height, urinary urea nitrogen, and feeding method in acutely ill adults. Using 2 evidence-based approaches, estimated protein needs were compared with laboratory-measured protein requirements. Comparisons were significantly associated for normal weight patients (r ¼ 0.21, P ¼ .03) but not for patients who were obese (r ¼ 0.10, P ¼ .49), showing that the use of body weight and standard formulas to calculate protein needs may not be appropriate for individuals who are obese. Considerations for individual patients should be considered. More research is needed to determine how to accurately estimate protein during acute illness in patients who are obese. Keywords: acutely ill adults, obesity, protein needs, urinary urea nitrogen Ó 2016 Elsevier, Inc. All rights reserved.
N
urse practitioners (NPs) in acute care settings are charged with providing safe and holistic care to increasingly complex patients. One facet of care is that NPs must have a working understanding of the nutritional needs of the acutely ill patient. In particular, the NP must understand protein needs, how those needs vary by body weight, and how protein usage is affected by acute illness. Even though the acute care NP may work in an interprofessional team with registered dietitians, the primary responsibility for the coordination of that care often falls to the NP. The application of standardized, disease-based protein recommendations to any acutely ill patient is problematic but is even more difficult in patients who are obese (body mass index [BMI] 30.0). Obesity is a disease state,1 which brings with it a chronic inflammatory process, increasing the need for adequate protein.2 Thus, there is a need to know if acutely ill patients who are obese have different protein needs when compared with those of normal weight. In addition, people who are obese may have comorbid conditions that warrant additional www.npjournal.org
considerations in the assessment and determination of protein needs. The obesity epidemic has challenged NPs to reassess old approaches to care and generate new standards of practice for patients who are obese. Improving clinical practice requires the use of evidence-based guidelines. Protein requirements in obesity and illness are not yet clearly established and are not well understood. Urinary urea nitrogen (UUN) can be used to estimate protein use during an acute illness, along with certain formulas designed to adjust for body weight. Thus, measuring UUN in people of differing body types (normal weight and obesity) may help to establish guidelines for estimating these needs. This retrospective chart review demonstrates an urgent need to examine how protein requirements for people who are obese could best be predicted. RESEARCH QUESTIONS
There are 2 research questions to consider. First, what is the relationship between body weight and dietary protein needs in acutely ill patients, as measured by a The Journal for Nurse Practitioners - JNP
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24-hour UUN test? Second, what is the relationship between measured protein needs and estimated protein needs in acutely ill patients who are obese? REVIEW OF THE LITERATURE
Protein is a vital macronutrient necessary for energy metabolism, digestion, blood clotting, vision, antibody formation, acid-base balance, and fluid regulation. It is also a key ingredient for growth, repair, and replacement of tissue.3 In times of illness and stress, adequate protein intake (or supplementation) can decrease the rate of muscle loss, improve immune function, and support recovery.4 Protein needs are associated with body composition, particularly obesity. An increase in adipose tissue results in a significant increase in body fat and a slight increase in lean body mass, which may affect these metabolic processes. Protein requirements for supporting health and promoting healing during an acute illness are well established for normal weight individuals5 (BMI, 18.5-24.9), yet there is a dearth of literature regarding protein requirements for obese patients (BMI 30.0).6,7 The first nitrogen balance studies, conducted as early as 1907, typically used small groups of healthy males who were of normal weight to determine the required protein needs to support general good health but not ill health.8,9 Nitrogen balance studies were then tailored for actual patient use in subsequent clinical studies that focused on specific disease states, thus generating protein recommendations (in g/kg) based on the patient diagnosis but not body weight.10,11 Protein needs are typically obtained in 1 of 2 ways. Measured needs are derived from laboratory tests. In the absence of measured needs, protein needs can be estimated using established calculations that incorporate factors such as height, weight, and injury. Currently, the most common laboratory test used to measure nitrogen balance in the clinical setting is a 24-hour UUN test.12 The UUN is a quick, simple, and inexpensive way to measure the catabolism of lean tissue and is the commonly accepted method of estimating nitrogen balance in clinical care patients.12-14 A 24-hour UUN test measures only the urea excreted in the urine; therefore, a standard formula has been developed to calculate protein loss from all sources using the results of the 24-hour 2
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UUN test with the addition of 4 g protein. This accounts for the loss of urea through feces, sweat, hair, skin, nails, creatinine, uric acid, and ammonia.15 In healthy subjects, UUN accounts for about 80% to 90% of urinary nitrogen losses, but illness stressors alter the production of urea and the results of the UUN test. Depending on the disease and type of stress, the amount of urinary urea accounted for by UUN can vary widely, falling well below or above the average.14 The urine collection technique and metabolic factors also affect the accuracy of 24-hour UUN results. For example, spills and leaking catheters result in inaccurate samples, and conditions such as edema, dialysis, renal insufficiency, and gastrointestinal bleeding alter test results.12,16 It is possible that a shorter collection period (6-12 hours) would help address some of these concerns.12 Despite the possible variances in UUN results, the test can still be used in conjunction with other assessment tools to monitor protein status and determine the best course of nutritional treatment for the patient.14 Current, well-developed protein guidelines specifically targeting acutely ill patients who are obese are lacking. Additionally, even fewer researchsupported recommendations for protein provision exist for critically ill patients who are obese and who may be receiving intentional hypocaloric feeding protocols. Guidelines suggest protein replacement of 2.0 g/kg ideal body weight (IBW) for patients with a BMI of 30.0 to 39.9 kg/m2 and 2.5 g/kg IBW for those with a BMI > 40.0 kg/m2.17 However, it is common practice to calculate a body weight adjustment in lieu of the patient’s actual body weight to estimate protein needs.6 The approaches include the use of IBW or adjusted body weight (ABW). The development and validation of body weight adjustment factors are not well documented. Data used to evaluate energy requirements are the basis for these body weight adjustment factors, yet little research supports their use in the determination of protein needs of patients who are obese.18,19 A common method for adjusting body weight in the United States is to calculate IBW using the Hamwi formula (males ¼ 106 pounds for the first 60 inches þ 6 pounds for every inch greater than 60 inches; females ¼ 100 pounds for the first 60 inches þ 5 pounds for every inch greater than 60 inches).18 Volume
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It is not clear how the formula was originally derived or whether it was ever well validated.18,19 The calculation of IBW uses only height and sex and does not account for an increase in fat-free mass (FFM). FFM is body mass comprised of approximately 75% water and 25% protein.20 ABW formulas, such as the Amato formula ([actual weight e IBW] 0.5 þ IBW), use IBW to calculate the protein needs to support FFM and then add an additional percent, typically 25% or 50% of the IBW, to account for the portion of metabolically active fat mass (fat in the adipose tissue).19,21 The purported intent of using ABW to estimate energy and protein needs in patients who are obese is to support the FFM, as well as a portion of the fat mass that is metabolically active.20,21 The original ABW formula first appeared in 1984, and it is uncertain how the formula for ABW was developed or if it is well validated.19,21 The Harris Benedict (HB) equation has been evaluated in obese populations, yet there remains a dearth of research about adjustment factors and estimated protein needs in patients who are obese. Two studies helped to establish the usefulness of the HB equation. In 1 study of women with normal and obese BMIs, the use of the HB equation combined with the actual body weight estimated energy needs with a 68% rate of accuracy. The underestimation of energy needs was 9%.22 When IBW was incorporated into the HB equation in lieu of the actual body weight, the opposite was found; energy needs were predicted accurately in 23% of cases, whereas energy needs were underestimated in 74% of the study participants. This shows the importance of the consideration of FFM. A similar study evaluated the precision of estimating energy needs in people who were obese using the HB equation with actual body weight versus using ABW (with adjustment factors of 25%).23 The results showed that energy needs were consistently underestimated when predicted by ABW in conjunction with the HB equation, and as BMI increased, the level of error in estimated needs also increased. When ABW (with adjustment factor) was used, there was a mean difference of 25% between measured and estimated energy needs in people who were obese. Additionally, in people with a BMI > 40.0 kg/m2, energy needs www.npjournal.org
were underestimated 100% of the time. When using actual body weight in the HB equation to calculate energy needs of people who were obese, the error rate was only 36%. In support of these findings, another group of researchers found the measured resting energy expenditure was significantly higher than the need estimated by the HB equation when IBW was included in the calculation.24 In summary, there appears to be a need for research that examines whether the estimation of protein needs in people who are obese should be based on actual body weight, IBW, or ABW. Therefore, the objectives of this study were to 1) investigate the relationship between body weight and dietary protein needs in acutely ill patients as measured by a 24-hour UUN test and 2) evaluate the relationship between measured protein needs and estimated protein needs in patients who were obese (using body weight adjustment factors in the predictive equations in lieu of actual body weight). METHODS
This study was a retrospective chart review of adult inpatients at a large facility in the Southeastern US. The study protocol received approval from the Institutional Review Boards for Human Subjects. Considering the variables in questions, a power analysis for a 2-sided hypothesis test with a significance level of 0.05 revealed that 150 charts were needed to achieve a power of 94%. A preliminary review of electronic medical records of patients on whom a UUN test had been collected during a single admission yielded a convenience sample of approximately 200 patients who fit the basic criteria. Considering the power analysis, number of charts available, and the reality that 25% of charts might be unusable because of study exclusion criteria, the goal for the sample size was set at 150 charts. Data collected from charts of 150 unique patients included age, sex, race, weight, height, a single UUN test result (as grams of nitrogen excreted) per admission, unit location at the time of UUN collection, feeding method, comorbidities, and admitting diagnosis. Weight at the time of admission and weight closest to the time of UUN collection were assessed, but only the weight closest to the UNN test was used for the calculation of body weight. The Journal for Nurse Practitioners - JNP
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The standard operating procedure at the facility was for daily weights to be taken on acute care units. Weights were taken using a bed scale and recorded in the medical record. The weight nearest the time of UUN collection was the weight used for analysis because a 24-hour UUN test was not always conducted on admission. Because this was a retrospective chart review, there was no way to determine the patients’ dry weight. The standard operating procedure for a 24-hour UUN test was to collect the urine sample in a 2-L container kept on ice in the patient’s room during the collection period. The start date and time and end date and time of the collection period were recorded in the medical record. Subjects were excluded if they were younger than 19 or older than 85 years of age, received hemodialysis at the time of UUN collection, had an insufficient urine volume (< 1.0 L) for UUN analysis, or were diagnosed with a gastrointestinal bleed or hepatic encephalopathy. For comparison of measured protein needs versus estimated protein requirements in patients who were obese, the IBW was calculated using the Hamwi formula, and ABW was calculated using the Amato formula.21 Subject charts were also coded with the BMI categories of normal weight, overweight, and obese as established by the World Health Organization.7 The majority (85.4%) of patients who were obese were within the BMI range of 30.0 and 39.9, and estimated protein requirements were calculated based on the recommendation of 2.0 g/kg for acutely ill patients who were obese (BMI ¼ 30.0-40.0 kg/m2) receiving hypocaloric feeding protocols.17 The results of the 24-hour UUN test were converted into grams of protein using the standardized formula ([24-hour UUN (g) þ 4 g] 6.25). Measured protein requirements determined from the results of UUN were then divided by actual weight, IBW, and ABW to generate a comparison of grams of protein per kilogram. Data Analysis
Descriptive characteristics (mean and standard deviation) were determined for the study population. Correlational analysis was used to evaluate the relationship of measured body weight with protein needs. There were 3 distinct outliers in the data set; 4
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therefore, the data analyses were run first with all subjects (N ¼ 150) and then subsequently without the 3 outliers. All subjects were included in the final analysis because the outcomes were the same for both analyses. Additional calculations estimated the precision (distance between the upper and lower confidence limits) of the 95% confidence interval for the Spearman rank correlation. This analysis showed a confidence interval width of 0.30. Paired Student t test and Spearman correlations assessed the relationship between estimated protein requirements using IBW, ABW, and measured protein requirements (UUN) in patients who were obese. Bland-Altman analyses graphically depicted agreement between protein requirements using IBW, ABW, and UUN in patients who were obese.25 All statistical tests were 2 tailed and performed using a significance level of < 0.05 using SAS (version 9.2, 2008; SAS Institute, Inc, Cary, NC). RESULTS
One hundred fifty subjects were included in the analyses, and the descriptive characteristics of the population are summarized in the Table. The study population was primarily comprised of white men, who were not of Hispanic or Latino ethnicity and ranged in age from 25 to 82 years of age (mean ¼ 61.9 10 years). Most subjects were between the ages of 50 and 69 and during admission were located in an intensive care unit at the time of the 24-hour UUN collection. Sources of nutrition at the time of specimen collection included parenteral nutrition, enteral nutrition, oral diet, or a combination of modalities. The number of patients who were not eating or receiving nutritional support included 2 underweight (BMI < 18.5), 4 normal weight (BMI ¼ 18.5-24.9), 4 overweight (BMI ¼ 25.0-29.9), and 3 obese (BMI ¼ 30.0-34.9) subjects. For the total group, the mean weight was 88.7 kg 26.9 kg, and the mean BMI was 26.9 7.7 kg/m2. The mean grams of protein excreted (UUN) was 95.6 35.4 g. Body weight was significantly associated with measured protein needs in the total group (r ¼ 0.29, P ¼ .0003) and in patients who were not obese (n ¼ 102, r ¼ 0.21, P ¼ .03; Figure 1). In patients who were obese, the measured protein needs were neither significantly associated with actual Volume
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Table. Demographic Data Variable
n
% Total
Range
Mean SD
Race White
82
54.7
Black or African American
62
41.3
Unknown
3
2.0
American Indian or Alaskan Native
2
1.3
Native Hawaiian or other Pacific Islander
1
0.7%
Sex Male Female
145
96.7
5
3.3
Age (years)
25-82
30
2
1.3
40-49
11
7.3
50-59
46
30.7
60-69
54
36.0
70-79
34
22.7
80
3
2.0
BMI
150
14.5-60.6
Underweight
20
13.3
14.5-18.49
Normal weight
47
31.3
18.5-24.9
Overweight
35
23.3
25.0-29.9
Obese
48
32.0
30.0-60.6
PO (per os)
23
15.3
TF
40
26.6
TPN
67
44.6
PO and TF
1
0.7
PO and TPN
1
0.7
TF and TPN
5
3.3
13
8.7
61.95 10.08
26.9 7.7
Feeding method
No nutrition support Weight (kg) used for 24-hour UUN
150
41.3-202.0
88.7 26.9
24-hour UUN results (grams of protein)
150
35.7-198.8
95.6 35.4
Underweight
20
41.2-184.3
92.0 40.1
Normal weight
47
38.1-182.0
85.8 30.4
Overweight
35
35.6-185.0
96.2 34.9
Obese
48
50.0-198.7
106.1 36.4
BMI ¼ body mass index; PO ¼ by mouth; SD ¼ standard deviation; TF ¼ tube feed; TPN ¼ total parenteral nutrition; UNN ¼ urinary urea nitrogen.
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Figure 1. Protein requirements as measured by urinary urea nitrogen excretion. 200
Protein (g)
150
100
Nonobese protein
50
Obese Linear (Nonobese protein) 0 25
45
65
85
105
125
145
165
185
205
225
Body weight (kg)
body weight (n ¼ 48, r ¼ 0.10, P ¼ .49; Figure 1), nor with estimated body weight using the body weight adjustment factors of IBW (r ¼ 0.02, P ¼ .86) or ABW (r ¼ 0.08, P ¼ .56). In the group of patients who were obese, the measured protein needs were 0.95 g/kg ( 0.38) of actual body weight. The predicted protein needs using IBW multiplied by 2.0 g/kg were higher and averaged 1.45 g/kg ( 0.52). The ABW multiplied by 2.0 g protein/kg was also higher and averaged 1.14 g/kg ( 0.42). Measured protein needs were significantly different from the protein needs predicted using IBW and ABW (P ¼ .001 for each), and the estimated protein needs typically overpredicted protein requirements (Figure 2). The use of IBW or ABW multiplied by 2.0 g protein/kg to predict protein requirements accurately predicted protein needs (within 10% of measured protein use) in 14.6% (n ¼ 7) and 8.3% (n ¼ 4; IBW and ABW, respectively) of the acutely
ill patients who were obese. Body weight adjustment factors used to predict protein requirements actually overpredicted (by > 110% of measured protein needs) in the majority of acutely ill patients who were obese. This overprediction occurred in 72.9% (n ¼ 35) when using IBW, 89.6% (n ¼ 43) when using ABW adjustments, and by 62.8 ( 24.9) and 93.8 ( 38.7) g protein when using the IBW and ABW, respectively. The error may occur because obesity represents a disproportionate ratio of leanto-fat mass, a criterion not present in the body weight adjustment calculation; thus, the use of those factors may represent incorrect assumptions about actual body composition in people who are obese.19 RECOMMENDATIONS
This study has implications for NPs, as well as other advanced practice nurses. The study shows that there is a need to consider how patients’ protein needs during acute illness are affected by body weight but may not be generalizable to well patients living in the community. For NPs providing care to acutely ill patients, these findings suggest that estimated protein needs based on either IBW or ABW are significantly different from the actual protein requirements of acutely ill patients who were obese. Interestingly, protein needs are typically greatly overestimated for this population. Because of the growing obesity epidemic, there is an urgent need to develop evidence-based guidelines specific to protein replacement in this population. Armed with this information, the NP helps provide consistency in
Figure 2. Bland-Altman plots.
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the standard of care and can engage the interprofessional team in meaningful discussions about dietary replacement of protein during acute illness. The objectives of this study were 2-fold. The primary objective was to investigate the relationship between BMI and measured protein needs (by 24-hour UUN) to determine if body weight was significantly associated with measured protein needs. A significant association between body weight and measured protein needs was observed for the entire group and in patients who were not obese but not the subset of patients who were obese. It is possible that the association between body weight and measured protein needs observed in the total group was driven by patients with normal BMIs. However, the study did suggest that the use of IBW and ABW calculation methods may be adequate for acutely ill adults who are not obese. This is an important consideration for acute care NPs working in interprofessional teams who are ordering nutritional support for acutely ill patients. The secondary study objective was to investigate the relationship between measured protein needs and estimated protein needs in patients who were obese by utilizing the IBW and ABW calculations commonly used in clinical practice. This study was unique in its assessment of the adequacy of estimation of protein needs based on predictive equations using IBW and ABW for patients who were obese. In examining the relationship between measured protein needs and adjusted body weight (IBW or ABW), this study found that measured protein needs were not associated with body weight in patients who were obese, even after using standard body weight adjustment factors. Additionally, we found that protein requirements as estimated by either IBW or ABW were significantly higher than measured protein needs (P < .001 for each). This study did have limitations. Similar to early nitrogen balance studies, our study population was comprised of a high percent of men, with charts of only 5 women available. Fluid imbalance alters both body weight and the relationship between measured and predicted protein needs, and the use of a retrospective chart review precluded the ability to assess patients for fluid overload. These factors may be seen as flaws to the design and may have www.npjournal.org
affected outcomes. To adjust for the unmet assumption of a normal distribution, Spearman correlations were used. One potential limitation may actually be a benefit of this study. Although most nitrogen balance studies focus on determining protein needs for patients with a particular disease state or at least stratify by disease state, this study did neither. Although not stratifying by disease state may have contributed to the variability in measured protein needs, the examination of results by BMI category lends strength to the study because it provides a more accurate representation of clinical practice and may, therefore, be more applicable across a range of disease states. To further explore the relationship between body weight and protein needs and to ensure that actual protein needs of acutely ill patients who are obese are being met, future research needs to be conducted. To offset the increased risk of error from a 24-hour UUN collection period, it has been suggested that a 6- or 12-hour collection period may be more effective.12 Studies should be prospective in nature and should control for caloric and fluid intake in addition to measuring protein excretion. The study population should be expanded to allow for the examination of various levels of protein provision, instead of 1 set provision rate; include an equal proportion of male and female subjects and ethnically diverse populations; and ensure all BMI categories are fully represented. CONCLUSIONS
The findings from previous studies22-24 and the current study support the position that using body weight adjustment factors to estimate nutritional needs may not correctly predict the true needs of patients. This study suggests that protein needs are directly associated with body weight in acutely ill patients with normal BMIs but that the same association is not seen for acutely ill patients who are obese. Additionally, protein needs calculated using adjustment factors such as IBW or ABW resulted in estimated needs that were not correlated with and were overestimates of measured needs. Acute care NPs should use interprofessional teams and, in particular, should seek the advice and The Journal for Nurse Practitioners - JNP
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expertise of the registered dietician on the team. When measurement of protein excretion to better determine actual protein requirements is unavailable, there may not be a clear advantage to using ABWs in estimating protein needs in the acutely ill patient who is obese. References 1. AMA. American Medical Association House of Delegates. Recognition of Obesity as a Disease. Resolution pp. 2. http://media.npr.org/documents/2013/ jun/ama-resolution-obesity.pdf. 2013. Accessed June 20, 2015. 2. Port AM, Apovian C. Metabolic support of the obese intensive care unit patient: a current perspective. Curr Opin Clin Nutr Metab Care. 2010;13:184-191. 3. Whitney E, Rolfes SR. Protein: amino acids. In: Adams P, ed. Understanding Nutrition. 11th ed. Belmont, CA: Thomas Wadsworth; 2008:180-203. 4. Winkler MF, Malone AM. Medical nutrition therapy for metabolic stress: sepsis, trauma, burns, and surgery. In: Mahan LK, Escott-Stump S, eds. Krause’s Food and Nutrition Therapy. 12th ed. Philadelphia, PA: Saunders Elsevier; 2008:1021-1041. 5. Institute of Medicine of the National Academies. Dietary Reference Intakes for Energy, Carbohydrates, Fiber, Fat, Protein, and Amino Acids (Macronutrients). Washington, DC: The National Academies Press; 2002/2005. 6. Ventura JM. Protein requirements and losses: surgical wounds and drains. Support Line. 2008;30:8-13. 7. Physical Status: The Use and Interpretation of Anthropometry. Report of a WHO Expert Committee (Technical Report Series No. 854). Geneva: World Health Organization; 1995:329. 8. Energy and Protein Requirements. Report of a Joint FAO/WHO Ad Hoc Expert Committee (Technical Report Series No. 522). Geneva: World Health Organization; 1973. 9. Bodwell CE, Schuster EM, Kyle E, et al. Obligatory urinary and fecal nitrogen losses in young women, older men, and young men and the factorial estimation of adult human protein requirements. Am J Clin Nutr. 1979;32:2450-2459. 10. Ishibashi N, Plank LD, Sando K, Hill G. Optimal protein requirements during the first 2 weeks after the onset of critical illness. Crit Care Med. 1998;26:1529-2459. 11. Swart GR, van den Berg JWO, van Vuure JK, Rietveld T, Wattimena DL, Frenkel M. Minimum protein requirements in liver cirrhosis determined by nitrogen balance measurements at three levels of protein intake. Clin Nutr. 1989;8:329-336. 12. Graves C, Saffle J, Morris S. Comparison of urine urea nitrogen collection times in critically ill patients. Nutr Clin Pract. 2005;20:271-275. 13. Bingham SA. Urine nitrogen as a biomarker for the validation of dietary protein intake. J Nutr. 2003;133:921S-924S. 14. Konstantidines FN. Nitrogen balance studies in clinical nutrition. Nutr Clin Pract. 1992;7:231-238. 15. Gropper SS, Smith JL, Groff JL. Protein. In: Gropper SS, Smith JL, Groff JL, eds. Advance Nutrition and Human Metabolism. 5th ed. Belmont, CA: Wadsworth CENGAGE Learning; 2009:179-250. 16. Heimburger DC. Nutrition Assessment. In: Heimburger DC, Ard JD, eds. Handbook of Clinical Nutrition. 4th ed. Philadelphia, PA: Mosby Elsevier; 2006:242-261. 17. Choban P, Dickerson R, Malone A, Worthington P, Compher C. American Society for Parenteral and Enteral Nutrition. A.S.P.E.N. Clinical guidelines: nutrition support of hospitalized adult patients with obesity. JPEN J Parenter Enteral Nutr. 2013;37:714-744.
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18. Shah B, Sucher K, Hollenbeck CB. Comparison of ideal body weight equations and published height-weight tables with body mass index tables for healthy adults in the United States. Nutr Clin Pract. 2006;21: 312-319. 19. Ireton-Jones C. Adjusted body weight, con: why adjust body weight in energy-expenditure calculations? Nutr Clin Pract. 2005;20:474-479. 20. Choban PS, Dickerson RN. Morbid obesity and nutrition support: is bigger different? Nutr Clin Pract. 2005;20:480-487. 21. Krenitsky J. Adjusted body weight, pro: evidence to support the use of adjusted body weight in calculation calorie requirements. Nutr Clin Pract. 2005;20:468-473. 22. Weijs PJM, Vansant GAAM. Validity of predictive equations for resting energy expenditure in Belgian normal weight to morbid obese women. Clin Nutr. 2010;29:347-351. 23. Frankenfield DC, Rowe WA, Smith JS, Cooney RN. Validation of several established equations for resting metabolic rate in obese and nonobese people. J Am Diet Assoc. 2003;103:1152-1159. 24. Feurer ID, Crosby LO, Buzby GP, Rosato EF, Mullen JL. Resting energy expenditure in morbid obesity. Ann Surg. 1983;197:17-21. 25. Bland JM, Altman DG. Measuring agreement in method comparison studies. Stat Methods Med Res. 1999;8:135-160.
Shannon McMahon, MS, RD, LD, is an instructor with the Department of Human Nutrition and Hospitality Management at The University of Alabama in Tuscaloosa. Linda Knol, PhD, RD, LD, is an associate professor at The University of Alabama. Alice L. March, PhD, FNP, CNE, is an assistant dean of graduate programs and associate professor with Capstone College of Nursing at The University of Alabama and can be reached at [email protected]. Jodie Bilbrey, MS, RD, is a retired clinical dietitian with the Department of Nutrition and Foodservices at the Veterans Department of Affairs Medical Center in Birmingham, AL. Sarah L. Morgan, MD, RD, FADA, FACP, is a professor of medicine and nutrition sciences and medical director at the UAB Osteoporosis Prevention and Treatment Clinic and Bone Densitometry Service in Birmingham, AL. Jeannine Lawrence, PhD, RD, LD, is an associate professor with the Department of Human Nutrition and Hospitality Management at the University of Alabama. In compliance with national ethical guidelines, the authors report no relationships with business or industry that would pose a conflict of interest. 1555-4155/16/$ see front matter © 2016 Elsevier, Inc. All rights reserved. http://dx.doi.org/10.1016/j.nurpra.2016.03.010
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