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Energy Expenditure in Hospitalized Patients: Implications for Nutritional Support
REVIEW
ENERGY EXPENDITURE IN HOSPITALIZED PATIENTS
Energy Expenditure in Hospitalized Patients: Implications for Nutritional Support JOHN M. MILES, MD An understanding of energy expenditure in hospitalized patients is necessary to determine optimal energy supply in the care of individuals who require nutritional support. A review was conducted of 19 studies in which resting energy expenditure (REE) had been measured using indirect calorimetry and compared with estimated basal energy expenditure (BEE) from the Harris-Benedict equation. Studies of patients with burns, head injuries, and fever were excluded because REE is known to be increased in these conditions. The studies reported data on 1256 patients with the following diagnoses: postoperative (28%), trauma or sepsis (26%), cancer (18%), pulmonary disease (9%), cardiovascular disease (2%), miscellaneous (9%), and unspecified (6%). The average REE in the 19 studies was 113% of the BEE. The mean ± SD REE/BEE ratio was higher in 11 studies in which the REE was measured during feeding than in 5 studies in which the measurement was made during fasting (117%±3% vs 105%±4%; P=.047). In those 11 studies, overfeeding may have contributed to higher REE values than otherwise would have been observed. Some evidence indicated that the REE/BEE ratio is higher in more severe illness, but results were inconsistent. Unfortunately, little information is available concerning total energy expenditure, which includes the contribution of physical activity. It appears that most patients can be fed adequately with energy equal to 100% to 120% of estimated BEE. Hypoenergetic feeding may be appropriate in some overweight and obese individuals. Additional research in hospitalized patients on total energy expenditure and on the relationship between severity of illness and energy expenditure is needed.
Mayo Clin Proc. 2006;81(6):809-816 APACHE = Acute Physiology and Chronic Health Evaluation; BEE = basal energy expenditure; REE = resting energy expenditure; TEE = total energy expenditure
N
utritional support is often given to hospitalized patients when illness interferes with normal food intake. However, uncertainty exists regarding when it should be used and how much should be given. Early work suggested that energy requirements are increased during illness to levels higher than those predicted for healthy individuals, in proportion to the severity of illness and degree of stress.1 More conservative estimates of energy expenditure, and thus energy requirements, have subsequently been adopted.2 However, a comprehensive review of studies in From the Endocrine Research Unit, Mayo Clinic College of Medicine, Rochester, Minn. This work was supported by grants from the US Public Health Service (HL67933) and the Mayo Foundation. Individual reprints of this article are not available. Address correspondence to John M. Miles, MD, Endocrine Research Unit, Mayo Clinic College of Medicine, 200 First St SW, Rochester, MN 55905 (e-mail: [email protected]). © 2006 Mayo Foundation for Medical Education and Research
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which energy expenditure was measured in hospitalized patients has not been conducted. Furthermore, the magnitude of the effect of stress and severity of illness on energy expenditure remains unclear. In this article, the results of such a review are presented, together with a discussion of the implications of the findings for nutritional care. The overall goals of the review were to (1) determine a best estimate of energy expenditure in hospitalized patients, (2) to investigate the effect of nutritional support on energy expenditure, and (3) to determine whether energy expenditure is increased in individuals with critical illnesses such as sepsis compared with individuals who are less critically ill. METHODS In a MEDLINE search, all studies of hospitalized patients in which resting energy expenditure (REE) had been measured with indirect calorimetry were identified. Search terms included REE, hospital, and critical illness. The review was confined to studies published since 1980 with a minimum of 20 patients in which REE was compared with estimated basal energy expenditure (BEE) determined by the Harris-Benedict equation.3 (The Harris-Benedict equations are BEE = 13.8W + 5H – 6.8A + 66.5 for males and BEE = 9.6W + 1.8H – 4.7A + 655 for females, where BEE is the BEE in kilocalories, W is the weight in kilograms, H is the height in centimeters, and A is the age in years.) Often, REE is considered to be synonymous with BEE, which represents the energy expenditure that occurs at complete rest after an overnight fast. For the purposes of this review, REE merely refers to a measurement of energy expenditure made in an inpatient; the measurement is sometimes made under fasting conditions and sometimes during feeding (see the “Results” section). In this review, studies of predominantly head injury or burn patients were excluded because these conditions are known to be accompanied by systematic increases in energy expenditure.4 When possible, febrile patients were excluded from analysis for the same reason. If the ratio of REE to BEE (hereafter referred to as REE/BEE and expressed in percentage) was not provided, it was calculated from available data. The coefficient of variation for REE/BEE was also calculated when possible. Information on whether the REE measurements were made during infusion of nutrients was
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ENERGY EXPENDITURE IN HOSPITALIZED PATIENTS
TABLE 1. Distribution of Diagnoses in 19 Studies of the Relationship Between Resting Energy Expenditure and Basal Energy Expenditure in Hospitalized Patients
Reference Askanazi et al7 Quebbeman et al8 Knox et al9 Baker et al10 Mann et al11 Weissman et al12 Foster et al13 Hunter et al14 Green et al15 Cortes & Nelson16 Liggett & Renfro17 Fredrix et al18 McMahon et al19 Brown et al20 Guenst & Nelson21 Boulanger et al22 Frankenfield et al23 Flancbaum et al24 Alexander et al25 Total (%)
Postoperative surgical diagnoses
Trauma
Sepsis
Respiratory failure
Cardiovascular disease
Pneumonia
Miscellaneous
Not reported
Total
0
3
11
0
0
0
0
18
0
32
10 0 2 0
5 0 4 0
6 0 8 0
0 0 0 0
0 0 1 6
2 200 0 14
2 0 5 0
19 0 0 27
0 0 0 4
44 200 20 51
40 22 15 0
0 0 0 7
0 44 0 7
0 0 0 7
0 0 0 0
0 10 0 0
0 1 3 0
0 20 2 0
0 3 0 0
40 100 20 21
25
6
0
0
0
0
0
0
0
31
0 65
0 0
18 0
9 0
20 0
0 0
11 0
0 0
15 0
73 65
55 0
0 0
0 17
0 0
0 0
0 0
0 0
0 11
0 42
55 70
84
0
20
23
1
0
4
0
8
140
0
115
0
0
0
0
0
0
0
115
22
23
8
11
3
0
0
0
0
67
13
4
7
0
0
0
0
12
0
36
42 92 (7)
0 31 (2)
7 79 (6)
76 1256 (100)
2 355 (28)
0 167 (13)
16 162 (13)
recorded since feeding has a thermic effect, producing an increase in energy expenditure.5 The amount of nutrition received was noted when it was available. In some cases, it was necessary to add the contribution of dietary protein to “nonprotein” calories to determine total energy supply. Information on diagnosis was recorded, and the studies were examined to determine whether there was evidence of a relationship between severity of illness and REE/BEE. Studies in which REE was measured during feeding were compared with those in which REE was measured in the fasting state to determine whether evidence existed for an effect of feeding on REE in hospitalized patients. RESULTS Twenty studies of energy expenditure in hospitalized patients that met the study criteria were identified. Of these studies, 1 was excluded because its results were more than 3 SDs from the mean.6 Diagnostic information on the patients studied from the remaining 19 studies7-25 is provided in Table 1. Among the 1256 patients described, 355 (28%) 810
Cancer
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0 226 (18)
0 26 (2)
9 118 (9)
were postoperative patients with a variety of surgical diagnoses. Another 329 (26%) had either trauma or sepsis. A total of 226 (18%) had a diagnosis of cancer, whereas 118 patients (9%) had pneumonia or respiratory failure. Nonsurgical cardiovascular conditions accounted for 31 patients (2%). Miscellaneous diagnoses, each less than 2% of the total, included bowel obstruction, pancreatitis, inflammatory bowel disease, enterocutaneous fistula, burns, renal failure, and bowel infarction. A diagnosis was not specified in 79 patients. A summary of feeding and energy expenditure data is given in Table 2. The REE data on individual patients was provided in only 2 studies.14,16 The mean REE/BEE in the 19 studies ranged from 94% to 130% and averaged 113%. Substantial intersubject variation occurred in REE/BEE in several of the reports. Patients were receiving nutrition at the time the REE was determined in 11 of the studies; in 8 of the studies, nutritional support provided energy equal to an average of 137% (range, 118%-165%) of the BEE 8,11,13,15,16,21,25 (J.M.M. and D. Frankenfield, MS, RD, written communi-
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ENERGY EXPENDITURE IN HOSPITALIZED PATIENTS
cation, April 2005), whereas in 3 studies the amount of nutrition was not stated.14,20,24 In 5 studies, patients were not receiving any nutrition at the time of the REE measurement, and in 1 study no information on nutritional status was available.22 Two studies were excluded from this aspect of the analysis because some of the patients were receiving nutritional support and some were not; REE data in the 2 groups were not provided separately.9,12 REE/BEE was higher in the 11 studies in which the measurement was made during nutrient infusion than in the 5 studies in which the measurement was made under fasting conditions (117%±3% vs 105%±4%; P=.047). A relationship between severity of illness and REE/BEE was not consistently observed, although the unavailability of individual REE/BEE data in most studies made it more difficult to examine this question. The mean ± SD REE/ BEE was 105%±5% in 4 studies in which an average of 36% of patients had sepsis and the measurement was made under fasting conditions,7,8,10,13,17 120%±6% in 4 studies in which an average of 25% of patients had sepsis but the measurements were made under fed conditions,15,20,24,25 and 116%±7% in 3 studies in which none of the patients had sepsis but the measurements were made under fed conditions.11,14,16 The differences in REE/BEE among these 3 groups of studies were not statistically significant. Foster et al13 found that REE/BEE was higher in 22 septic patients than in 78 nonseptic patients (111%±13% vs 103%±16%; P=.02). Liggett et al17 reported that REE was 29% higher than BEE in 18 septic patients (P<.0001) and only 13% higher than BEE in 51 nonseptic patients (P=NS). Therefore, in these 2 studies, REE/BEE was 8% and 14% higher in septic patients than in nonseptic patients, respectively. Another study reported a significant correlation between REE/BEE and Acute Physiology and Chronic Health Evaluation (APACHE) II score in critically ill patients.20 DISCUSSION For many years, it has been suggested that energy expenditure, and thus energy requirement, is increased in hospitalized patients. In 1979, Long et al1 reported that hospitalized patients had systematic increases in increased energy expenditure or hypermetabolism; in that study, REE/BEE ranged from 124% for those having elective surgery to 179% for those with sepsis. The use of stress factors to account for such hypermetabolism was subsequently widely adopted, and stress factors are still used today in many centers. However, the results of the current review indicate that these older estimates of energy expenditure are probably inaccurate. When individuals with fever, burns, and head injuries are excluded, the mean REE/BEE in hospitalized patients is approximately 113%. Mayo Clin Proc.
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TABLE 2. Measured vs Predicted Energy Expenditure in Hospitalized Patients*
Reference Askanazi et al Quebbeman et al8 Knox et al9 Baker at al10 Mann et al11 Weissman et al12 Foster et al13 Hunter et al14 Green et al15 Cortes & Nelson16 Liggett & Renfro17 Fredrix et al18 McMahon et al19 Brown et al20 Guenst & Nelson21 Boulanger et al22 Frankenfield et al23 Flancbaum et al24 Alexander et al25 Mean (SD)
7
Fed
(REE/BEE) × 100 (%)
Coefficient of variation (%)
32
No
94
NR
44 200 20 51
Yes NR No Yes
106 99 102 115
12 19 29 NR
40 100 20 21
NR Yes Yes Yes
104 105 104 121
21 14 39 5
31
Yes
128
19
73 65
No No
117 110
10 8
55 70
No Yes
102 115
26 NR
140
Yes
120
17
115
NR
124
26
67
Yes
124
14
36
Yes
130
NR
76
Yes
126 113.0 (10.9)
27
No. of patients
*BEE is the estimated basal energy expenditure calculated using the Harris-Benedict equation. REE is the resting energy expenditure measured by indirect calorimetry. NR = not reported.
The relationship between severity of illness and REE/ BEE is not entirely clear. It is well established that individuals with burns are hypermetabolic, with REE/BEE values of 140% to 150%.26 Muscular activity appears to be at least partly responsible for the overall increase in energy expenditure in burn patients.27 A similar observation has been made in patients with head trauma; REE/BEE ranges from 120% to 145% for 2 to 3 weeks after injury.28-33 Hypermetabolism in this group of patients appears to be due to posturing and hypertonicity.28,32,33 Thus, increased muscular activity contributes to greater than predicted energy expenditure in both burn and head injury patients. A distinction should be made between an effect of illness severity per se vs an effect of elevated body temperature, which has long been associated with increased energy expenditure. Lusk34 estimated that energy expenditure increased 11% with each 1.0°C elevation of body temperature. A more recent study reported a nearly identical relationship between fever and REE in patients with head injury.35 Moreover, cooling of febrile patients has been
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ENERGY EXPENDITURE IN HOSPITALIZED PATIENTS
shown to produce an approximately 10% reduction in REE per degree Celsius.36 In the current analysis, an attempt was made to exclude febrile individuals. However, temperature status was not provided in most of the studies. REE/BEE data were presented separately in febrile and afebrile patients only in the study by Frankenfield et al23; the febrile patients were excluded from the analysis. Therefore, it is possible that the presence of fever in some of the 1256 patients studied could have increased the REE/BEE in those individuals. Factors other than fever and increased muscular activity can mediate increases in energy expenditure in critically ill patients. Infusions of glucagon,37 catecholamines,38 growth hormone,39 and cortisol40 have each been shown to cause acute increases in REE, averaging 10% to 15% above baseline. The thermic effect of increases in the concentrations of these hormones, all of which promote a generalized increase in fuel availability, may be due to activation of energy-requiring processes such as gluconeogenesis and ureagenesis. Increased free fatty acid availability may also be a factor.41 Whether increases in 2 or more of these stress hormones have an additive or even synergistic effect on energy expenditure is not known. When head injury, burns, and fever are excluded, conflicting data remain concerning REE/BEE in hospitalized patients. One textbook refers to a “20% to 50% increase in REE in critically ill patients.”42 Another textbook describes a 50% increase in patients with multiple injuries and energy expenditure that can reach “50 to 60% above normal” in sepsis.43 There is some basis for these assertions. REE/ BEE values of 155% to 191% have been reported in patients with sepsis.44,45 In both those studies, patients were febrile and receiving nutritional support at the time of the REE measurement. In 2 other studies, patients with sepsis had REE/BEE values that were only 8% and 14% higher than in nonseptic individuals.13,17 Askanazi et al7 reported REE/BEE values of 114% in a group of trauma and sepsis patients, compared with 79% in depleted patients with weight loss. Brown et al20 measured the REE in critically ill patients and found that REE/BEE was 124% in a quintile (19%) of patients with the highest APACHE II scores, whereas it was 88% to 106% in the remainder of individuals with lower APACHE II scores. However, another large study found no relationship between REE/BEE and APACHE II score.46 In the current review, studies in which sepsis was well represented did not have higher REE/BEE values than studies in which there were no septic patients. Thus, data on the relationship between severity of illness and hypermetabolism are inconsistent. It appears that when fever, head injury, and burns are excluded, the magnitude of the increase in REE/BEE among severely ill hospitalized patients is uncertain and may be relatively small. 812
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A confounding factor that limits interpretation of published data is the possibility of technical error in the REE measurement. An accurate determination of REE requires an experienced operator who is familiar with the various pitfalls that can introduce errors, including calibration problems, non–steady-state conditions, and cuff leaks.47-50 Considerable intersubject variability in REE/BEE has been reported in some studies (Table 2). Vermeij et al51 performed continuous indirect calorimetry in patients receiving mechanical ventilatory support for 2 to 7 consecutive days and found within-subject variability as high as 31%, which was reduced only slightly when a correction for body temperature was made. The authors stated that factors such as sedation, muscle relaxation, and changes in nutritional support could account for the remaining variability. However, an alternative explanation for such within-subject variability is imprecision in the measurement due to technical limitations. Others have reported that day-to-day within-subject variability in REE is much greater in a group of critically ill patients compared with individuals who were more stable clinically.12 Technical issues could also be partly responsible for the between-subject variability indicated in Table 2. In addition to causing imprecision in the measurement, technical problems can produce systematic errors. Use of non–steady-state data in a calculation, for example, could result in either systematic overestimates or underestimates of REE. Data from an individual report must be interpreted with caution because of the possibility of such errors. In the current study, there was a surprisingly wide range in REE/ BEE among the 19 studies reviewed, differences that were not consistently related to severity of illness. Although some of the differences in reported REE/BEE in sepsis (ranging from 110%13 to 129%17 to 165%6 to 191%45) may be due to differences in the definition of this condition,52 technical errors could also be a factor. Energy expenditure data in healthy outpatient controls would be reassuring in this regard, but such data are almost universally absent in the published literature on inpatients. The results of the current review suggest that administration of nutritional support increases REE/BEE, which was significantly higher (P=.047) when the REE measurement was made during feeding (11 studies) than when it was made in the fasting state (5 studies). This difference in REE/BEE is not surprising and presumably reflects the thermic effect of feeding. Considering that the thermic effect of nutrients is greater with higher rates of feeding53 and that patients in several of the studies were fed at 145% of BEE or higher,11,13,16 these rates of energy expenditure (and in turn the energy requirements they purport to represent) may be greater than would occur when patients are fed at lower rates. In other words, if the expectation of
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ENERGY EXPENDITURE IN HOSPITALIZED PATIENTS
hypermetabolism54 leads to overfeeding, it may to some extent be self-fulfilling. Do published estimates of energy expenditure, based on relatively brief, one-time measurements made with indirect calorimetry, represent actual energy requirements? It should be remembered that energy expenditure has 3 components: BEE, thermic effect of food, and activity thermogenesis. Therefore, the sum of these 3 components will represent the energy supply needed for energy equilibrium. The 11 studies in which REE was determined during feeding provide measures of the sum of the first 2 of these, BEE plus the thermic effect of feeding, although as indicated herein, the average REE in these studies (117%) may overestimate what would occur if overfeeding were avoided. Even when performed during feeding, REE measurements do not take physical activity into account. For this reason, it has been suggested that an activity factor should be applied in calculating energy supply.55 However, critically ill patients are for the most part inactive. Procedures such as chest physiotherapy, repositioning, weighing, bathing, and other activities can temporarily increase REE by 20% to 35%.56 However, the impact of this phenomenon is relatively minor; even if the activities occupied 6 hours of the day, the result would be a less than 5% increase in 24-hour energy expenditure. Swinamer et al57 found that intensive care unit activities accounted for only 1% to 4% to total energy expenditure (TEE), measured during 24 hours, in critically ill patients. Another study found that energy expenditure can increase by approximately 100% after a percutaneous muscle biopsy.58 However, the duration of the increase averaged only 11 minutes.58 Because the REE measurement does not take activity thermogenesis into account, it underestimates actual 24hour TEE. Unfortunately, relatively few data are available on measurements of TEE in hospitalized patients. Excluding studies of burns and head injury, we found only 3 studies in which TEE had been measured in hospitalized adults. Carlsson et al59 reported TEE/BEE values averaging 125% in a group of critically ill patients, using continuous indirect calorimetry for an average of 6 days during feeding that provided an average of 126% of BEE. Novick et al60 measured TEE in 7 patients with Crohn disease, using the doubly labeled water method. They also measured REE with indirect calorimetry. REE/BEE was 109% before surgery and 108% after surgery. However, TEE/BEE was approximately 120% immediately before surgery and approximately 140% when measured again 7 days later. It is difficult to explain the marked increase in TEE in the postoperative measurement in that study, but it may be due to an artifact. Measuring carbon dioxide production twice in rapid succession in the same individual with doubly labeled water is difficult because asMayo Clin Proc.
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sumptions are required concerning the decay of tracer enrichment that originates from the initial dose. These assumptions are needed to subtract this “background” to determine the enrichment from the second dose. If the assumptions are wrong, an error is introduced. Therefore, the postoperative TEE values from that study are of questionable accuracy. In another study, 24-hour REE was measured in a whole-body calorimeter, and TEE was determined with doubly labeled water in 8 inpatients with Crohn disease who were receiving parenteral nutrition.61 These investigators reported that REE/BEE and TEE/ BEE averaged 108% and 131%, respectively. The difference between REE and TEE in that study is presumably primarily due to physical activity since some of the patients were ambulatory.61 The patients in both these studies received large amounts of parenteral feeding equal to 164%60 and 186%61 of BEE. What influence should these observations have on feeding practices in the hospital? The American College of Chest Physicians has recommended feeding intensive care patients at a rate of 25 kcal/kg daily.2 Table 3 shows calculated BEE in examples of young and old and lean and obese men and women compared with energy supply using American College of Chest Physicians guidelines. As can be seen, feeding according to these guidelines results in underfeeding in young, lean individuals and overfeeding in elderly, obese people. This is not surprising, considering that the increase in energy expenditure that occurs with weight gain is not a linear function of body weight.62 Some investigators have advocated the use of an “adjusted” body weight to avoid this kind of error.63 However, the use of actual weight in a formula that reflects actual energy expenditure, such as the Harris-Benedict equation, is preferable in our view. The BEE derived from the HarrisBenedict equation was used in this review as a denominator to express measured energy expenditure data because it is by far the most widely used comparator in studies reporting REE in hospitalized patients. This does not mean that the Harris-Benedict equation is the only way to calculate energy requirements. A number of other methods,64 including a popular Web site (http://epen.kumc.edu/), have been used for this purpose. Isoenergetic feeding for most inpatients (excluding those with burns, closed head injury, and fever), especially those who are not ambulatory, would fall in the range of 100% to 120% of estimated BEE (Harris-Benedict equation) based on the results of this review. In overweight and obese patients, hypoenergetic feeding may be desirable to minimize hyperglycemia, hypertriglyceridemia, and sodium retention.65-69 Hypoenergetic feeding in overweight and obese individuals is typically provided at a rate of 70% to 80% of estimated BEE, calculated from the Harris-
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TABLE 3. Estimates of Energy Expenditure From the Harris-Benedict Equation Compared With Energy Supply Based on the ACCP Guidelines* Example No./ sex/age (y)
Height (cm)
Weight (kg)
BEE (kcal/d)
ACCP (kcal/d)
ACCP (% BEE)
1/M/20 2/F/20 3/M/20 4/F/20 5/M/75 6/F/75 7/M/75 8/F/75
178 160 178 160 178 160 178 160
56 45 114 92 56 45 114 92
1592 1288 2390 1737 1221 1031 2018 1480
1400 1125 2850 2300 1550 1125 2850 2300
88 87 119 132 127 109 141 155
*ACCP = American College of Chest Physicians; BEE = basal energy expenditure.
Benedict equation using actual weight. A case can be made for erring on the side of hypoenergetic feeding in all patients, considering that most individuals who require nutritional support have adequate fat stores that readily mobilize free fatty acids to provide energy to fat-burning tissues. Critically ill patients have surprisingly high free fatty acid concentrations and rates of fat oxidation, even when receiving parenteral nutrition that contains large amounts of glucose.70 This observation indicates that adipose tissue lipolysis is resistant to the antilipolytic effects of insulin during severe illness, a phenomenon likely mediated by augmented release of stress hormones. This nonsuppressible endogenous lipid should be considered as available fuel, together with nutrients delivered exogenously. In the same respect, isoenergetic feeding does not prevent negative nitrogen balance in critically ill patients.71 Markedly hyperenergetic feeding can accomplish this goal,72 but the cost may be hyperglycemia and hyperlipidemia, contributing to adverse outcomes. Overfeeding in general is associated with impaired immune function.73 To the extent that overfeeding has been the historical standard of care in the United States, it may be partly responsible for the adverse outcomes that have been reported from parenteral nutrition in large clinical studies.74-77 Although parsimony is appropriate when feeding most patients, depleted individuals represent an exception because they have minimal fat stores and are therefore vulnerable to underfeeding. Moreover, they often tolerate increases in energy supply with minimal or no hyperglycemia and hypertriglyceridemia. CONCLUSION When burns, head injuries, and fever are excluded, the REE in hospitalized patients averages approximately 113% of the BEE calculated from the Harris-Benedict equation. The impact of illness severity on the REE is uncertain but may be relatively small. Administration of 814
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nutritional support increases the REE by approximately 11%, although this effect might be less when overfeeding is avoided. The overall effect of physical activity on TEE in the critically ill individual confined to bed is small, and its contribution to the TEE in ambulatory hospitalized individuals is uncertain. Further research on TEE in hospitalized patients, ideally using a high-quality technique such as doubly labeled water, is needed. Additional studies on the relationship between energy expenditure and illness severity should be conducted. Most patients (excluding those with burns, closed head injury, and fever) can be fed adequately by supplying 100% to 120% of the estimated BEE (Harris-Benedict equation). Higher rates may be needed in ambulatory individuals, especially those who are depleted. I thank Steven B. Heymsfield, MD, William L. Isley, MD, James A. Levine, MD, PhD, M. Molly McMahon, MD, and Robert A. Rizza, MD, for helpful comments. I also acknowledge the late C. R. Fleming, MD, whose commitment to nutritional care inspired all who knew him.
REFERENCES 1. Long CL, Schaffel N, Geiger JW, Schiller WR, Blakemore WS. Metabolic response to injury and illness: estimation of energy and protein needs from indirect calorimetry and nitrogen balance. JPEN J Parenter Enteral Nutr. 1979;3:452-456. 2. Cerra FB, Benitez MR, Blackburn GL, et al. Applied nutrition in ICU patients: a consensus statement of the American College of Chest Physicians. Chest. 1997;111:769-778. 3. Harris JA, Benedict FG. A Biometric Study of Basal Metabolism in Man. Washington, DC: Carnegie Institute of Washington; 1919. 4. Miles JM. Nutritional support in stroke: a balanced meal or a feast? [editorial]. Neurocrit Care. 2004;1:283-286. 5. Segal KR, Gutin B. Thermic effects of food and exercise in lean and obese women. Metabolism. 1983;32:581-589. 6. Hwang TL, Huang SL, Chen MF. The use of indirect calorimetry in critically ill patients—the relationship of measured energy expenditure to Injury Severity Score, Septic Severity Score, and APACHE II Score. J Trauma. 1993; 34:247-251. 7. Askanazi J, Carpentier YA, Elwyn DH, et al. Influence of total parenteral nutrition on fuel utilization in injury and sepsis. Ann Surg. 1980;191:40-46.
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ENERGY EXPENDITURE IN HOSPITALIZED PATIENTS
8. Quebbeman EJ, Ausman RK, Schneider TC. A re-evaluation of energy expenditure during parenteral nutrition. Ann Surg. 1982;195:282-286. 9. Knox LS, Crosby LO, Feurer ID, Buzby GP, Miller CL, Mullen JL. Energy expenditure in malnourished cancer patients. Ann Surg. 1983;197:152162. 10. Baker JP, Detsky AS, Stewart S, Whitwell J, Marliss EB, Jeejeebhoy KN. Randomized trial of total parenteral nutrition in critically ill patients: metabolic effects of varying glucose-lipid ratios as the energy source. Gastroenterology. 1984;87:53-59. 11. Mann S, Westenskow DR, Houtchens BA. Measured and predicted caloric expenditure in the acutely ill. Crit Care Med. 1985;13:173-177. 12. Weissman C, Kemper M, Askanazi J, Hyman AI, Kinney JM. Resting metabolic rate of the critically ill patient: measured versus predicted. Anesthesiology. 1986;64:673-679. 13. Foster GD, Knox LS, Dempsey DT, Mullen JL. Caloric requirements in total parenteral nutrition. J Am Coll Nutr. 1987;6:231-253. 14. Hunter DC, Jaksic T, Lewis D, Benotti PN, Blackburn GL, Bistrian BR. Resting energy expenditure in the critically ill: estimations versus measurement. Br J Surg. 1988;75:875-878. 15. Green CJ, McClelland P, Gilbertson AA, WIlkes RG, Bone JM, Campbell IT. Energy balance in acute illness [abstract]. Proc Nutr Soc. 1989; 48:73A. 16. Cortes V, Nelson LD. Errors in estimating energy expenditure in critically ill surgical patients. Arch Surg. 1989;124:287-290. 17. Liggett SB, Renfro AD. Energy expenditures of mechanically ventilated nonsurgical patients. Chest. 1990;98:682-686. 18. Fredrix EW, Soeters PB, von Meyenfeldt MF, Saris WH. Resting energy expenditure in cancer patients before and after gastrointestinal surgery. JPEN J Parenter Enteral Nutr. 1991;15:604-607. 19. McMahon MM, Farnell MB, Murray MJ. Nutritional support of critically ill patients. Mayo Clin Proc. 1993;68:911-920. 20. Brown PE, McClave SA, Hoy NW, Short AF, Sexton LK, Meyer KL. The Acute Physiology and Chronic Health Evaluation II classification system is a valid marker for physiologic stress in the critically ill patient. Crit Care Med. 1993;21:363-367. 21. Guenst JM, Nelson LD. Predictors of total parenteral nutrition-induced lipogenesis. Chest. 1994;105:553-559. 22. Boulanger BR, Nayman R, McLean RF, Phillips E, Rizoli SB. What are the clinical determinants of early energy expenditure in critically injured adults? J Trauma. 1994;37:969-974. 23. Frankenfield DC, Smith JS Jr, Cooney RN, Blosser SA, Sarson GY. Relative association of fever and injury with hypermetabolism in critically ill patients. Injury. 1997;28:617-621. 24. Flancbaum L, Choban PS, Sambucco S, Verducci J, Burge JC. Comparison of indirect calorimetry, the Fick method, and prediction equations in estimating the energy requirements of critically ill patients. Am J Clin Nutr. 1999;69:461-466. 25. Alexander E, Susla GM, Burstein AH, Brown DT, Ognibene FP. Retrospective evaluation of commonly used equations to predict energy expenditure in mechanically ventilated, critically ill patients. Pharmacotherapy. 2004;24:1659-1667. 26. Rutan TC, Herndon DN, Van Osten T, Abston S. Metabolic rate alterations in early excision and grafting versus conservative treatment. J Trauma. 1986;26:140-142. 27. Goran MI, Peters EJ, Herndon DN, Wolfe RR. Total energy expenditure in burned children using the doubly labeled water technique. Am J Physiol. 1990;259(4, pt 1):E576-E585. 28. Clifton GL, Robertson CS, Choi SC. Assessment of nutritional requirements of head-injured patients. J Neurosurg. 1986;64:895-901. 29. Fried RC, Dickerson RN, Guenter PA, et al. Barbiturate therapy reduces nitrogen excretion in acute head injury. J Trauma. 1989;29:15581564. 30. Young B, Ott L, Norton J, et al. Metabolic and nutritional sequelae in the non-steroid treated head injury patient. Neurosurgery. 1985;17:784791. 31. Weekes E, Elia M. Observations on the patterns of 24-hour energy expenditure changes in body composition and gastric emptying in head-injured patients receiving nasogastric tube feeding. JPEN J Parenter Enteral Nutr. 1996;20:31-37.
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32. Borzotta AP, Pennings J, Papasadero B, et al. Enteral versus parenteral nutrition after severe closed head injury. J Trauma. 1994;37:459-468. 33. Robertson CS, Clifton GL, Grossman RG. Oxygen utilization and cardiovascular function in head-injured patients. Neurosurgery. 1984;15:307314. 34. Lusk G. The Elements of the Science of Nutrition. 4th ed. Philadelphia, Pa: WB Saunders; 1928. 35. Bruder N, Raynal M, Pellissier D, Courtinat C, Francois G. Influence of body temperature, with or without sedation, on energy expenditure in severe head-injured patients. Crit Care Med. 1998;26:568-572. 36. Manthous CA, Hall JB, Olson D, et al. Effect of cooling on oxygen consumption in febrile critically ill patients. Am J Respir Crit Care Med. 1995; 151:10-14. 37. Nair KS. Hyperglucagonemia increases resting metabolic rate in man during insulin deficiency. J Clin Endocrinol Metab. 1987;64:896-901. 38. Ratheiser KM, Brillon DJ, Campbell RG, Matthews DE. Epinephrine produces a prolonged elevation in metabolic rate in humans. Am J Clin Nutr. 1998;68:1046-1052. 39. Wolthers T, Groftne T, Moller N, et al. Calorigenic effects of growth hormone: the role of thyroid hormones. J Clin Endocrinol Metab. 1996;81: 1416-1419. 40. Brillon DJ, Zheng B, Campbell RG, Matthews DE. Effect of cortisol on energy expenditure and amino acid metabolism in humans. Am J Physiol. 1995;268(3, pt 1):E501-E513. 41. Sbraccia P, D’Adamo M, Leonetti F, et al. Relationship between plasma free fatty acids and uncoupling protein-3 gene expression in skeletal muscle of obese subjects: in vitro evidence of a causal link. Clin Endocrinol (Oxf). 2002; 57:199-207. 42. Mowatt-Larssen C, Brown R. Drug-nutrient interactions. In: Zaloga GP, ed. Nutrition in Critical Care. St Louis, Mo: Mosby; 1994:487-503. 43. Souba WW, Wilmore DW. Diet and nutrition in the care of the patient with surgery, trauma, and sepsis. In: Shils ME, Olson JA, Shike M, Ross AC, eds. Modern Nutrition in Health and Disease. 9th ed. Baltimore, Md: Williams & Wilkins; 1999:1589-1618. 44. Kreymann G, Grosser S, Buggisch P, Gottschall C, Matthaei S, Greten H. Oxygen consumption and resting metabolic rate in sepsis, sepsis syndrome, and septic shock. Crit Care Med. 1993;21:1012-1019. 45. Frankenfield DC, Wiles CE III, Bagley S, Siegel JH. Relationships between resting and total energy expenditure in injured and septic patients. Crit Care Med. 1994;22:1796-1804. 46. Swinamer DL, Grace MG, Hamilton SM, Jones RL, Roberts P, King EG. Predictive equation for assessing energy expenditure in mechanically ventilated critically ill patients. Crit Care Med. 1990;18:657661. 47. Ruppel GL. Manual of Pulmonary Function Testing. 8th ed. St Louis, Mo: Mosby; 2003:338-347. 48. Brandi LS, Bertolini R, Calafa M. Indirect calorimetry in critically ill patients: clinical applications and practical advice. Nutrition. 1997;13:349358. 49. Rasanen J. Continuous breathing circuit flow and tracheal tube cuff leak: sources of error during pediatric indirect calorimetry. Crit Care Med. 1992; 20:1335-1340. 50. McClave SA, Snider HL. Use of indirect calorimetry in clinical nutrition. Nutr Clin Pract. 1992;7:207-221. 51. Vermeij CG, Feenstra BW, van Lanschot JJ, Bruining HA. Day-to-day variability of energy expenditure in critically ill surgical patients. Crit Care Med. 1989;17:623-626. 52. Calandra T, Cohen J, International Sepsis Forum Definition of Infection in the ICU Consensus Conference. The international sepsis forum consensus conference on definitions of infection in the intensive care unit. Crit Care Med. 2005;33:1538-1548. 53. Segal KR, Edano A, Blando L, Pi-Sunyer FX. Comparison of thermic effects of constant and relative caloric loads in lean and obese men. Am J Clin Nutr. 1990;51:14-21. 54. Long CL, Blakemore WS. Energy and protein requirements in the hospitalized patient. JPEN J Parenter Enteral Nutr. 1979;3:69-71. 55. Clevenger FW, Rodriguez DJ, Demarest GB, Osler TM, Olson SE, Fry DE. Protein and energy tolerance by stressed geriatric patients. J Surg Res. 1992;52:135-139.
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56. Weissman C, Kemper M, Damask MC, Askanazi J, Hyman AI, Kinney JM. Effect of routine intensive care interactions on metabolic rate. Chest. 1984; 86:815-818. 57. Swinamer DL, Phange PT, Jones RL, Grace M, King EG. Twenty-four hour energy expenditure in critically ill patients. Crit Care Med. 1987;15:637643. 58. Damask MC, Askanazi J, Weissman C, Elwyn DH, Kinney JM. Artifacts in measurement of resting energy expenditure. Crit Care Med. 1983;11:750-752. 59. Carlsson M, Nordenstrom J, Hedenstierna G. Clinical implications of continuous measurement of energy expenditure in mechanically ventilated patients. Clin Nutr. 1984;3:103-110. 60. Novick WM, Nusbaum M, Stein TP. The energy costs of surgery as measured by the doubly labeled water (2H218O) method. Surgery. 1988; 103:99-106. 61. Pullicino E, Coward A, Elia M. Total energy expenditure in intravenously fed patients measured by the doubly labeled water technique. Metabolism. 1993;42:58-64. 62. Jequier E. Energy expenditure in obesity. Clin Endocrinol Metab. 1984; 13:563-580. 63. Barak N, Wall-Alonso E, Sitrin MD. Evaluation of stress factors and body weight adjustments currently used to estimate energy expenditure in hospitalized patients. JPEN J Parenter Enteral Nutr. 2002;26:231238. 64. Frankenfield DC, Rowe WA, Smith JS, Cooney RN. Validation of several established equations for resting metabolic rate in obese and nonobese people [published correction appears in J Am Diet Assoc. 2003;103:1593]. J Am Diet Assoc. 2003;103:1152-1159. 65. Dickerson RN, Rosato EF, Mullen JL. Net protein anabolism with hypocaloric parenteral nutrition in obese stressed patients. Am J Clin Nutr. 1986; 44:747-755. 66. Baxter JK, Bistrian BR. Moderate hypocaloric parenteral nutrition in the critically ill, obese patient. Nutr Clin Pract. 1989;4:133-135. 67. Burge JC, Goon A, Choban PS, Flancbaum L. Efficacy of hypocaloric total parenteral nutrition in hospitalized obese patients: a prospective,
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double-blind randomized trial. JPEN J Parenter Enteral Nutr. 1994;18:203207. 68. Choban PS, Burge JC, Scales D, Flancbaum L. Hypoenergetic nutrition support in hospitalized obese patients: a simplified method for clinical application. Am J Clin Nutr. 1997;66:546-550. 69. Liu KJ, Cho MJ, Atten MJ, et al. Hypocaloric parenteral nutrition support in elderly obese patients. Am Surg. 2000;66:394-399. 70. Stoner HB, Little RA, Frayn KN, Elebute AE, Tresadern J, Gross E. The effect of sepsis on the oxidation of carbohydrate and fat. Br J Surg. 1983;70: 32-35. 71. Frankenfield DC, Smith JS, Cooney RN. Accelerated nitrogen loss after traumatic injury is not attenuated by achievement of energy balance. JPEN J Parenter Enteral Nutr. 1997;21:324-329. 72. Rutten P, Blackburn GL, Flatt JP, Hallowell E, Cochran D. Determination of optimal hyperalimentation infusion rate. J Surg Res. 1975;18:477483. 73. Chandra RK. Immunodeficiency in undernutrition and overnutrition. Nutr Rev. 1981;39:225-231. 74. Veterans Affairs Total Parenteral Nutrition Cooperative Study Group. Perioperative total parenteral nutrition in surgical patients. N Engl J Med. 1991;325:525-532. 75. Klein S, Kinney J, Jeejeebhoy K, et al. Nutrition support in clinical practice: review of published data and recommendations for future research directions: summary of a conference sponsored by the National Institutes of Health, American Society for Parenteral and Enteral Nutrition, and American Society for Clinical Nutrition. Am J Clin Nutr. 1997;66:683706. 76. Braunschweig CL, Levy P, Sheean PM, Wang X. Enteral compared with parenteral nutrition: a meta-analysis. Am J Clin Nutr. 2001;74:534542. 77. Gramlich L, Kichian K, Pinilla J, Rodych NJ, Dhaliwal R, Heyland DK. Does enteral nutrition compared to parenteral nutrition result in better outcomes in critically ill adult patients? a systematic review of the literature. Nutrition. 2004;20:843-848.
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ENERGY EXPENDITURE IN HOSPITALIZED PATIENTS
Energy Expenditure in Hospitalized Patients: Implications for Nutritional Support JOHN M. MILES, MD An understanding of energy expenditure in hospitalized patients is necessary to determine optimal energy supply in the care of individuals who require nutritional support. A review was conducted of 19 studies in which resting energy expenditure (REE) had been measured using indirect calorimetry and compared with estimated basal energy expenditure (BEE) from the Harris-Benedict equation. Studies of patients with burns, head injuries, and fever were excluded because REE is known to be increased in these conditions. The studies reported data on 1256 patients with the following diagnoses: postoperative (28%), trauma or sepsis (26%), cancer (18%), pulmonary disease (9%), cardiovascular disease (2%), miscellaneous (9%), and unspecified (6%). The average REE in the 19 studies was 113% of the BEE. The mean ± SD REE/BEE ratio was higher in 11 studies in which the REE was measured during feeding than in 5 studies in which the measurement was made during fasting (117%±3% vs 105%±4%; P=.047). In those 11 studies, overfeeding may have contributed to higher REE values than otherwise would have been observed. Some evidence indicated that the REE/BEE ratio is higher in more severe illness, but results were inconsistent. Unfortunately, little information is available concerning total energy expenditure, which includes the contribution of physical activity. It appears that most patients can be fed adequately with energy equal to 100% to 120% of estimated BEE. Hypoenergetic feeding may be appropriate in some overweight and obese individuals. Additional research in hospitalized patients on total energy expenditure and on the relationship between severity of illness and energy expenditure is needed.
Mayo Clin Proc. 2006;81(6):809-816 APACHE = Acute Physiology and Chronic Health Evaluation; BEE = basal energy expenditure; REE = resting energy expenditure; TEE = total energy expenditure
N
utritional support is often given to hospitalized patients when illness interferes with normal food intake. However, uncertainty exists regarding when it should be used and how much should be given. Early work suggested that energy requirements are increased during illness to levels higher than those predicted for healthy individuals, in proportion to the severity of illness and degree of stress.1 More conservative estimates of energy expenditure, and thus energy requirements, have subsequently been adopted.2 However, a comprehensive review of studies in From the Endocrine Research Unit, Mayo Clinic College of Medicine, Rochester, Minn. This work was supported by grants from the US Public Health Service (HL67933) and the Mayo Foundation. Individual reprints of this article are not available. Address correspondence to John M. Miles, MD, Endocrine Research Unit, Mayo Clinic College of Medicine, 200 First St SW, Rochester, MN 55905 (e-mail: [email protected]). © 2006 Mayo Foundation for Medical Education and Research
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which energy expenditure was measured in hospitalized patients has not been conducted. Furthermore, the magnitude of the effect of stress and severity of illness on energy expenditure remains unclear. In this article, the results of such a review are presented, together with a discussion of the implications of the findings for nutritional care. The overall goals of the review were to (1) determine a best estimate of energy expenditure in hospitalized patients, (2) to investigate the effect of nutritional support on energy expenditure, and (3) to determine whether energy expenditure is increased in individuals with critical illnesses such as sepsis compared with individuals who are less critically ill. METHODS In a MEDLINE search, all studies of hospitalized patients in which resting energy expenditure (REE) had been measured with indirect calorimetry were identified. Search terms included REE, hospital, and critical illness. The review was confined to studies published since 1980 with a minimum of 20 patients in which REE was compared with estimated basal energy expenditure (BEE) determined by the Harris-Benedict equation.3 (The Harris-Benedict equations are BEE = 13.8W + 5H – 6.8A + 66.5 for males and BEE = 9.6W + 1.8H – 4.7A + 655 for females, where BEE is the BEE in kilocalories, W is the weight in kilograms, H is the height in centimeters, and A is the age in years.) Often, REE is considered to be synonymous with BEE, which represents the energy expenditure that occurs at complete rest after an overnight fast. For the purposes of this review, REE merely refers to a measurement of energy expenditure made in an inpatient; the measurement is sometimes made under fasting conditions and sometimes during feeding (see the “Results” section). In this review, studies of predominantly head injury or burn patients were excluded because these conditions are known to be accompanied by systematic increases in energy expenditure.4 When possible, febrile patients were excluded from analysis for the same reason. If the ratio of REE to BEE (hereafter referred to as REE/BEE and expressed in percentage) was not provided, it was calculated from available data. The coefficient of variation for REE/BEE was also calculated when possible. Information on whether the REE measurements were made during infusion of nutrients was
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ENERGY EXPENDITURE IN HOSPITALIZED PATIENTS
TABLE 1. Distribution of Diagnoses in 19 Studies of the Relationship Between Resting Energy Expenditure and Basal Energy Expenditure in Hospitalized Patients
Reference Askanazi et al7 Quebbeman et al8 Knox et al9 Baker et al10 Mann et al11 Weissman et al12 Foster et al13 Hunter et al14 Green et al15 Cortes & Nelson16 Liggett & Renfro17 Fredrix et al18 McMahon et al19 Brown et al20 Guenst & Nelson21 Boulanger et al22 Frankenfield et al23 Flancbaum et al24 Alexander et al25 Total (%)
Postoperative surgical diagnoses
Trauma
Sepsis
Respiratory failure
Cardiovascular disease
Pneumonia
Miscellaneous
Not reported
Total
0
3
11
0
0
0
0
18
0
32
10 0 2 0
5 0 4 0
6 0 8 0
0 0 0 0
0 0 1 6
2 200 0 14
2 0 5 0
19 0 0 27
0 0 0 4
44 200 20 51
40 22 15 0
0 0 0 7
0 44 0 7
0 0 0 7
0 0 0 0
0 10 0 0
0 1 3 0
0 20 2 0
0 3 0 0
40 100 20 21
25
6
0
0
0
0
0
0
0
31
0 65
0 0
18 0
9 0
20 0
0 0
11 0
0 0
15 0
73 65
55 0
0 0
0 17
0 0
0 0
0 0
0 0
0 11
0 42
55 70
84
0
20
23
1
0
4
0
8
140
0
115
0
0
0
0
0
0
0
115
22
23
8
11
3
0
0
0
0
67
13
4
7
0
0
0
0
12
0
36
42 92 (7)
0 31 (2)
7 79 (6)
76 1256 (100)
2 355 (28)
0 167 (13)
16 162 (13)
recorded since feeding has a thermic effect, producing an increase in energy expenditure.5 The amount of nutrition received was noted when it was available. In some cases, it was necessary to add the contribution of dietary protein to “nonprotein” calories to determine total energy supply. Information on diagnosis was recorded, and the studies were examined to determine whether there was evidence of a relationship between severity of illness and REE/BEE. Studies in which REE was measured during feeding were compared with those in which REE was measured in the fasting state to determine whether evidence existed for an effect of feeding on REE in hospitalized patients. RESULTS Twenty studies of energy expenditure in hospitalized patients that met the study criteria were identified. Of these studies, 1 was excluded because its results were more than 3 SDs from the mean.6 Diagnostic information on the patients studied from the remaining 19 studies7-25 is provided in Table 1. Among the 1256 patients described, 355 (28%) 810
Cancer
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0 226 (18)
0 26 (2)
9 118 (9)
were postoperative patients with a variety of surgical diagnoses. Another 329 (26%) had either trauma or sepsis. A total of 226 (18%) had a diagnosis of cancer, whereas 118 patients (9%) had pneumonia or respiratory failure. Nonsurgical cardiovascular conditions accounted for 31 patients (2%). Miscellaneous diagnoses, each less than 2% of the total, included bowel obstruction, pancreatitis, inflammatory bowel disease, enterocutaneous fistula, burns, renal failure, and bowel infarction. A diagnosis was not specified in 79 patients. A summary of feeding and energy expenditure data is given in Table 2. The REE data on individual patients was provided in only 2 studies.14,16 The mean REE/BEE in the 19 studies ranged from 94% to 130% and averaged 113%. Substantial intersubject variation occurred in REE/BEE in several of the reports. Patients were receiving nutrition at the time the REE was determined in 11 of the studies; in 8 of the studies, nutritional support provided energy equal to an average of 137% (range, 118%-165%) of the BEE 8,11,13,15,16,21,25 (J.M.M. and D. Frankenfield, MS, RD, written communi-
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ENERGY EXPENDITURE IN HOSPITALIZED PATIENTS
cation, April 2005), whereas in 3 studies the amount of nutrition was not stated.14,20,24 In 5 studies, patients were not receiving any nutrition at the time of the REE measurement, and in 1 study no information on nutritional status was available.22 Two studies were excluded from this aspect of the analysis because some of the patients were receiving nutritional support and some were not; REE data in the 2 groups were not provided separately.9,12 REE/BEE was higher in the 11 studies in which the measurement was made during nutrient infusion than in the 5 studies in which the measurement was made under fasting conditions (117%±3% vs 105%±4%; P=.047). A relationship between severity of illness and REE/BEE was not consistently observed, although the unavailability of individual REE/BEE data in most studies made it more difficult to examine this question. The mean ± SD REE/ BEE was 105%±5% in 4 studies in which an average of 36% of patients had sepsis and the measurement was made under fasting conditions,7,8,10,13,17 120%±6% in 4 studies in which an average of 25% of patients had sepsis but the measurements were made under fed conditions,15,20,24,25 and 116%±7% in 3 studies in which none of the patients had sepsis but the measurements were made under fed conditions.11,14,16 The differences in REE/BEE among these 3 groups of studies were not statistically significant. Foster et al13 found that REE/BEE was higher in 22 septic patients than in 78 nonseptic patients (111%±13% vs 103%±16%; P=.02). Liggett et al17 reported that REE was 29% higher than BEE in 18 septic patients (P<.0001) and only 13% higher than BEE in 51 nonseptic patients (P=NS). Therefore, in these 2 studies, REE/BEE was 8% and 14% higher in septic patients than in nonseptic patients, respectively. Another study reported a significant correlation between REE/BEE and Acute Physiology and Chronic Health Evaluation (APACHE) II score in critically ill patients.20 DISCUSSION For many years, it has been suggested that energy expenditure, and thus energy requirement, is increased in hospitalized patients. In 1979, Long et al1 reported that hospitalized patients had systematic increases in increased energy expenditure or hypermetabolism; in that study, REE/BEE ranged from 124% for those having elective surgery to 179% for those with sepsis. The use of stress factors to account for such hypermetabolism was subsequently widely adopted, and stress factors are still used today in many centers. However, the results of the current review indicate that these older estimates of energy expenditure are probably inaccurate. When individuals with fever, burns, and head injuries are excluded, the mean REE/BEE in hospitalized patients is approximately 113%. Mayo Clin Proc.
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TABLE 2. Measured vs Predicted Energy Expenditure in Hospitalized Patients*
Reference Askanazi et al Quebbeman et al8 Knox et al9 Baker at al10 Mann et al11 Weissman et al12 Foster et al13 Hunter et al14 Green et al15 Cortes & Nelson16 Liggett & Renfro17 Fredrix et al18 McMahon et al19 Brown et al20 Guenst & Nelson21 Boulanger et al22 Frankenfield et al23 Flancbaum et al24 Alexander et al25 Mean (SD)
7
Fed
(REE/BEE) × 100 (%)
Coefficient of variation (%)
32
No
94
NR
44 200 20 51
Yes NR No Yes
106 99 102 115
12 19 29 NR
40 100 20 21
NR Yes Yes Yes
104 105 104 121
21 14 39 5
31
Yes
128
19
73 65
No No
117 110
10 8
55 70
No Yes
102 115
26 NR
140
Yes
120
17
115
NR
124
26
67
Yes
124
14
36
Yes
130
NR
76
Yes
126 113.0 (10.9)
27
No. of patients
*BEE is the estimated basal energy expenditure calculated using the Harris-Benedict equation. REE is the resting energy expenditure measured by indirect calorimetry. NR = not reported.
The relationship between severity of illness and REE/ BEE is not entirely clear. It is well established that individuals with burns are hypermetabolic, with REE/BEE values of 140% to 150%.26 Muscular activity appears to be at least partly responsible for the overall increase in energy expenditure in burn patients.27 A similar observation has been made in patients with head trauma; REE/BEE ranges from 120% to 145% for 2 to 3 weeks after injury.28-33 Hypermetabolism in this group of patients appears to be due to posturing and hypertonicity.28,32,33 Thus, increased muscular activity contributes to greater than predicted energy expenditure in both burn and head injury patients. A distinction should be made between an effect of illness severity per se vs an effect of elevated body temperature, which has long been associated with increased energy expenditure. Lusk34 estimated that energy expenditure increased 11% with each 1.0°C elevation of body temperature. A more recent study reported a nearly identical relationship between fever and REE in patients with head injury.35 Moreover, cooling of febrile patients has been
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ENERGY EXPENDITURE IN HOSPITALIZED PATIENTS
shown to produce an approximately 10% reduction in REE per degree Celsius.36 In the current analysis, an attempt was made to exclude febrile individuals. However, temperature status was not provided in most of the studies. REE/BEE data were presented separately in febrile and afebrile patients only in the study by Frankenfield et al23; the febrile patients were excluded from the analysis. Therefore, it is possible that the presence of fever in some of the 1256 patients studied could have increased the REE/BEE in those individuals. Factors other than fever and increased muscular activity can mediate increases in energy expenditure in critically ill patients. Infusions of glucagon,37 catecholamines,38 growth hormone,39 and cortisol40 have each been shown to cause acute increases in REE, averaging 10% to 15% above baseline. The thermic effect of increases in the concentrations of these hormones, all of which promote a generalized increase in fuel availability, may be due to activation of energy-requiring processes such as gluconeogenesis and ureagenesis. Increased free fatty acid availability may also be a factor.41 Whether increases in 2 or more of these stress hormones have an additive or even synergistic effect on energy expenditure is not known. When head injury, burns, and fever are excluded, conflicting data remain concerning REE/BEE in hospitalized patients. One textbook refers to a “20% to 50% increase in REE in critically ill patients.”42 Another textbook describes a 50% increase in patients with multiple injuries and energy expenditure that can reach “50 to 60% above normal” in sepsis.43 There is some basis for these assertions. REE/ BEE values of 155% to 191% have been reported in patients with sepsis.44,45 In both those studies, patients were febrile and receiving nutritional support at the time of the REE measurement. In 2 other studies, patients with sepsis had REE/BEE values that were only 8% and 14% higher than in nonseptic individuals.13,17 Askanazi et al7 reported REE/BEE values of 114% in a group of trauma and sepsis patients, compared with 79% in depleted patients with weight loss. Brown et al20 measured the REE in critically ill patients and found that REE/BEE was 124% in a quintile (19%) of patients with the highest APACHE II scores, whereas it was 88% to 106% in the remainder of individuals with lower APACHE II scores. However, another large study found no relationship between REE/BEE and APACHE II score.46 In the current review, studies in which sepsis was well represented did not have higher REE/BEE values than studies in which there were no septic patients. Thus, data on the relationship between severity of illness and hypermetabolism are inconsistent. It appears that when fever, head injury, and burns are excluded, the magnitude of the increase in REE/BEE among severely ill hospitalized patients is uncertain and may be relatively small. 812
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A confounding factor that limits interpretation of published data is the possibility of technical error in the REE measurement. An accurate determination of REE requires an experienced operator who is familiar with the various pitfalls that can introduce errors, including calibration problems, non–steady-state conditions, and cuff leaks.47-50 Considerable intersubject variability in REE/BEE has been reported in some studies (Table 2). Vermeij et al51 performed continuous indirect calorimetry in patients receiving mechanical ventilatory support for 2 to 7 consecutive days and found within-subject variability as high as 31%, which was reduced only slightly when a correction for body temperature was made. The authors stated that factors such as sedation, muscle relaxation, and changes in nutritional support could account for the remaining variability. However, an alternative explanation for such within-subject variability is imprecision in the measurement due to technical limitations. Others have reported that day-to-day within-subject variability in REE is much greater in a group of critically ill patients compared with individuals who were more stable clinically.12 Technical issues could also be partly responsible for the between-subject variability indicated in Table 2. In addition to causing imprecision in the measurement, technical problems can produce systematic errors. Use of non–steady-state data in a calculation, for example, could result in either systematic overestimates or underestimates of REE. Data from an individual report must be interpreted with caution because of the possibility of such errors. In the current study, there was a surprisingly wide range in REE/ BEE among the 19 studies reviewed, differences that were not consistently related to severity of illness. Although some of the differences in reported REE/BEE in sepsis (ranging from 110%13 to 129%17 to 165%6 to 191%45) may be due to differences in the definition of this condition,52 technical errors could also be a factor. Energy expenditure data in healthy outpatient controls would be reassuring in this regard, but such data are almost universally absent in the published literature on inpatients. The results of the current review suggest that administration of nutritional support increases REE/BEE, which was significantly higher (P=.047) when the REE measurement was made during feeding (11 studies) than when it was made in the fasting state (5 studies). This difference in REE/BEE is not surprising and presumably reflects the thermic effect of feeding. Considering that the thermic effect of nutrients is greater with higher rates of feeding53 and that patients in several of the studies were fed at 145% of BEE or higher,11,13,16 these rates of energy expenditure (and in turn the energy requirements they purport to represent) may be greater than would occur when patients are fed at lower rates. In other words, if the expectation of
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ENERGY EXPENDITURE IN HOSPITALIZED PATIENTS
hypermetabolism54 leads to overfeeding, it may to some extent be self-fulfilling. Do published estimates of energy expenditure, based on relatively brief, one-time measurements made with indirect calorimetry, represent actual energy requirements? It should be remembered that energy expenditure has 3 components: BEE, thermic effect of food, and activity thermogenesis. Therefore, the sum of these 3 components will represent the energy supply needed for energy equilibrium. The 11 studies in which REE was determined during feeding provide measures of the sum of the first 2 of these, BEE plus the thermic effect of feeding, although as indicated herein, the average REE in these studies (117%) may overestimate what would occur if overfeeding were avoided. Even when performed during feeding, REE measurements do not take physical activity into account. For this reason, it has been suggested that an activity factor should be applied in calculating energy supply.55 However, critically ill patients are for the most part inactive. Procedures such as chest physiotherapy, repositioning, weighing, bathing, and other activities can temporarily increase REE by 20% to 35%.56 However, the impact of this phenomenon is relatively minor; even if the activities occupied 6 hours of the day, the result would be a less than 5% increase in 24-hour energy expenditure. Swinamer et al57 found that intensive care unit activities accounted for only 1% to 4% to total energy expenditure (TEE), measured during 24 hours, in critically ill patients. Another study found that energy expenditure can increase by approximately 100% after a percutaneous muscle biopsy.58 However, the duration of the increase averaged only 11 minutes.58 Because the REE measurement does not take activity thermogenesis into account, it underestimates actual 24hour TEE. Unfortunately, relatively few data are available on measurements of TEE in hospitalized patients. Excluding studies of burns and head injury, we found only 3 studies in which TEE had been measured in hospitalized adults. Carlsson et al59 reported TEE/BEE values averaging 125% in a group of critically ill patients, using continuous indirect calorimetry for an average of 6 days during feeding that provided an average of 126% of BEE. Novick et al60 measured TEE in 7 patients with Crohn disease, using the doubly labeled water method. They also measured REE with indirect calorimetry. REE/BEE was 109% before surgery and 108% after surgery. However, TEE/BEE was approximately 120% immediately before surgery and approximately 140% when measured again 7 days later. It is difficult to explain the marked increase in TEE in the postoperative measurement in that study, but it may be due to an artifact. Measuring carbon dioxide production twice in rapid succession in the same individual with doubly labeled water is difficult because asMayo Clin Proc.
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sumptions are required concerning the decay of tracer enrichment that originates from the initial dose. These assumptions are needed to subtract this “background” to determine the enrichment from the second dose. If the assumptions are wrong, an error is introduced. Therefore, the postoperative TEE values from that study are of questionable accuracy. In another study, 24-hour REE was measured in a whole-body calorimeter, and TEE was determined with doubly labeled water in 8 inpatients with Crohn disease who were receiving parenteral nutrition.61 These investigators reported that REE/BEE and TEE/ BEE averaged 108% and 131%, respectively. The difference between REE and TEE in that study is presumably primarily due to physical activity since some of the patients were ambulatory.61 The patients in both these studies received large amounts of parenteral feeding equal to 164%60 and 186%61 of BEE. What influence should these observations have on feeding practices in the hospital? The American College of Chest Physicians has recommended feeding intensive care patients at a rate of 25 kcal/kg daily.2 Table 3 shows calculated BEE in examples of young and old and lean and obese men and women compared with energy supply using American College of Chest Physicians guidelines. As can be seen, feeding according to these guidelines results in underfeeding in young, lean individuals and overfeeding in elderly, obese people. This is not surprising, considering that the increase in energy expenditure that occurs with weight gain is not a linear function of body weight.62 Some investigators have advocated the use of an “adjusted” body weight to avoid this kind of error.63 However, the use of actual weight in a formula that reflects actual energy expenditure, such as the Harris-Benedict equation, is preferable in our view. The BEE derived from the HarrisBenedict equation was used in this review as a denominator to express measured energy expenditure data because it is by far the most widely used comparator in studies reporting REE in hospitalized patients. This does not mean that the Harris-Benedict equation is the only way to calculate energy requirements. A number of other methods,64 including a popular Web site (http://epen.kumc.edu/), have been used for this purpose. Isoenergetic feeding for most inpatients (excluding those with burns, closed head injury, and fever), especially those who are not ambulatory, would fall in the range of 100% to 120% of estimated BEE (Harris-Benedict equation) based on the results of this review. In overweight and obese patients, hypoenergetic feeding may be desirable to minimize hyperglycemia, hypertriglyceridemia, and sodium retention.65-69 Hypoenergetic feeding in overweight and obese individuals is typically provided at a rate of 70% to 80% of estimated BEE, calculated from the Harris-
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TABLE 3. Estimates of Energy Expenditure From the Harris-Benedict Equation Compared With Energy Supply Based on the ACCP Guidelines* Example No./ sex/age (y)
Height (cm)
Weight (kg)
BEE (kcal/d)
ACCP (kcal/d)
ACCP (% BEE)
1/M/20 2/F/20 3/M/20 4/F/20 5/M/75 6/F/75 7/M/75 8/F/75
178 160 178 160 178 160 178 160
56 45 114 92 56 45 114 92
1592 1288 2390 1737 1221 1031 2018 1480
1400 1125 2850 2300 1550 1125 2850 2300
88 87 119 132 127 109 141 155
*ACCP = American College of Chest Physicians; BEE = basal energy expenditure.
Benedict equation using actual weight. A case can be made for erring on the side of hypoenergetic feeding in all patients, considering that most individuals who require nutritional support have adequate fat stores that readily mobilize free fatty acids to provide energy to fat-burning tissues. Critically ill patients have surprisingly high free fatty acid concentrations and rates of fat oxidation, even when receiving parenteral nutrition that contains large amounts of glucose.70 This observation indicates that adipose tissue lipolysis is resistant to the antilipolytic effects of insulin during severe illness, a phenomenon likely mediated by augmented release of stress hormones. This nonsuppressible endogenous lipid should be considered as available fuel, together with nutrients delivered exogenously. In the same respect, isoenergetic feeding does not prevent negative nitrogen balance in critically ill patients.71 Markedly hyperenergetic feeding can accomplish this goal,72 but the cost may be hyperglycemia and hyperlipidemia, contributing to adverse outcomes. Overfeeding in general is associated with impaired immune function.73 To the extent that overfeeding has been the historical standard of care in the United States, it may be partly responsible for the adverse outcomes that have been reported from parenteral nutrition in large clinical studies.74-77 Although parsimony is appropriate when feeding most patients, depleted individuals represent an exception because they have minimal fat stores and are therefore vulnerable to underfeeding. Moreover, they often tolerate increases in energy supply with minimal or no hyperglycemia and hypertriglyceridemia. CONCLUSION When burns, head injuries, and fever are excluded, the REE in hospitalized patients averages approximately 113% of the BEE calculated from the Harris-Benedict equation. The impact of illness severity on the REE is uncertain but may be relatively small. Administration of 814
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nutritional support increases the REE by approximately 11%, although this effect might be less when overfeeding is avoided. The overall effect of physical activity on TEE in the critically ill individual confined to bed is small, and its contribution to the TEE in ambulatory hospitalized individuals is uncertain. Further research on TEE in hospitalized patients, ideally using a high-quality technique such as doubly labeled water, is needed. Additional studies on the relationship between energy expenditure and illness severity should be conducted. Most patients (excluding those with burns, closed head injury, and fever) can be fed adequately by supplying 100% to 120% of the estimated BEE (Harris-Benedict equation). Higher rates may be needed in ambulatory individuals, especially those who are depleted. I thank Steven B. Heymsfield, MD, William L. Isley, MD, James A. Levine, MD, PhD, M. Molly McMahon, MD, and Robert A. Rizza, MD, for helpful comments. I also acknowledge the late C. R. Fleming, MD, whose commitment to nutritional care inspired all who knew him.
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