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Original Communication

Journal of Parenteral and Enteral


Nutrition
Continuous Indirect Calorimetry in Critically Injured Patients Volume 44 Number 5
July 2020 889–894
Reveals Significant Daily Variability and Delayed, Sustained 
C 2019 American Society for

Parenteral and Enteral Nutrition


Hypermetabolism DOI: 10.1002/jpen.1713
wileyonlinelibrary.com

Georgia Vasileiou, MD1 ; Michelle B. Mulder, MD1 ; Sinong Qian, MD1 ;


Rahul Iyengar, BS1 ; Lindsey M. Gass, RD2 ; Jonathan Parks, MD1 ;
Edward Lineen, MD1 ; Patricia Byers, MD1 ; and Daniel Dante Yeh, MD1

Abstract
Background: Previous studies have used using Indirect Calorimetry (IC) with solitary or sparse measurements of resting energy
expenditure (REE). This “snapshot” may not capture the dynamic nature of metabolic requirements. Using continuous IC, we
describe the variation of REE during the first days in the intensive care unit. Methods: Injured adults (ࣙ18 years) requiring
mechanical ventilation from March 2018 to September 2018 were enrolled. IC was initiated within 4 days of admission and
continuous REE recorded until 14 days, extubation, or death. Multiple 10-minute periods collected during steady state were used to
calculate daily REE maximum, minimum, average, and variability [(REEmax − REEmin/2)/average REE]. Results: We included 55
patients. Median age was 38 [27–58] years, 38 (69%) were male, body mass index was 28 [25–33] kg/m2 , and Acute Physiology and
Chronic Health Evaluation II was 17 [14–24]. Mechanism of injury was: blunt (n = 38, 69%), penetrating (n = 9, 16%), and burn
(n = 8, 15%). Average REE increased gradually from 1,663 kcal [1,435–2,143] to a maximum of 2,080 [1,701–2,336] on day 7, a
relative 25% increase, which was sustained through day 14. REE variability ranged 8%–13% and was not reliably predicted by fever,
tachycardia, elevated intracranial pressures, hypertension, or hypotension. Conclusion: In critically injured patients, steady-state
REE measurements display fluctuations over a 24-hour period and demonstrate a gradual rise over the first few days after injury.
Continuous REE, if available, is recommended for more precise matching of energy delivery to metabolic requirements. (JPEN J
Parenter Enteral Nutr. 2020;44:889–894)

Keywords
adult; calorimetry; outcomes research/quality; surgery; trauma

Clinical Relevancy Statement rarely repeated; however, it has been shown that REE can
vary considerably within a 24-hour period and between
The use of indirect calorimetry (IC) as a clinical gold days.6,7 Thus, when short-interval measurements of REE
standard remains unchallenged, but continuous measure- are extrapolated to calculate a patient’s 24-hour total energy
ment of energy expenditure has been extremely limited.
The majority of the studies published so far use single
IC measurements taken at varying times during hospital- From the 1 Miller School of Medicine, DeWitt Daughtry Family
ization. In this study, we collected continuous calorimetry Department of Surgery, University of Miami, Miami, Florida, USA;
measurements during the first 14 days of intensive care unit and 2 Nutrition Services, Jackson Memorial Hospital, Miami, Florida,
admission, describe the daily variability that energy expen- USA.
diture exhibits in critically injured patients, and describe its Financial disclosure: D. D. Yeh receives author royalties by
relationship with clinical events. UpToDate. D. D. Yeh and P. Byers have separate Takeda research
grants. The rest of the authors have no financial disclosures.

Introduction Conflicts of interest: None declared.


Received for publication March 14, 2019; accepted for publication
Indirect calorimetry (IC) remains the gold standard for August 28, 2019.
measuring resting energy expenditure (REE) in critically This article originally appeared online on October 10, 2019.
ill patients.1 In practice, IC is used to assess the metabolic
Corresponding Author:
response to various states, such as burns,2,3 head injury,4 and Georgia Vasileiou, MD, University of Miami, 1800 NW 10th Ave,
fever,5 to design energy-provision regimens. In the literature, T-215, Miami, FL 33136, USA.
most REE measurements are performed only once or only Email: georgia.vas@gmail.com
890 Journal of Parenteral and Enteral Nutrition 44(5)

expenditure (TEE), significant error can result in over- or sedation. It is the customary practice of the ICU dietitians
undernourishment of hospitalized patients. As a result, it is to review the average amount of propofol received and
suggested that measurements should be taken during steady deduct the propofol energy from the energy targets during
state.8-10 reassessments. Therefore, we did not include propofol en-
Critically injured patients experience significant changes ergy in our deficits, as it would have been double-counted.
in clinical status and metabolic requirements over the course Multiple 10-minute periods were collected daily during
of hospitalization in response to medical/nursing care or steady state (coefficient of variation ࣘ 5% for both
complications. Considering patients with highly variable oxygen consumption (VO2 ) and carbon dioxide production
hospital courses, optimal care may depend upon repeated (VCO2 )) and were used to calculate REE daily maximum,
IC measurements throughout a patient’s entire stay.11,12 REE daily minimum, REE daily average, and REE
Therefore, in trauma, a single 24-hour IC measurement may variability [(REEmax − REEmin/2)/average REE]. The
not adequately capture the dynamic nature of a patient’s CARESCAPE R-860 collects metabolic information in
metabolic requirements. However, there are limited data a continuous fashion, and these data are stored for up
among trauma patients of continuous IC measurements to 24 hours. Every day, the previous day’s record was
beyond a 24-hour period. In this study, we sought to reviewed for any 10-minute steady-state time periods (as
continuously measure the IC of trauma patients in the defined above). A minimum of 4 periods of 10 minutes
intensive care unit (ICU) over the initial 2-week period were chosen, and attempts were made to select time periods
to examine the within-day and between-day variations of dispersed throughout the day. Variability calculation was
REE. We hypothesized that the metabolic requirements of based on all 10-minute periods recorded for that day, and
trauma ICU patients would change considerably during the number of periods used to calculated variability was
early hospitalization. dependent upon the number of recorded 10-minute periods
for that day. For the maximum and minimum REE values
that were collected, we recorded clinical events occurring at
Methods that time (fever > 38.5°C, intracranial pressure > 15 mmHg,
Following approval from our institutional review board, we heart rate > 120 beats/min, systolic blood pressure [BP]
prospectively enrolled injured adults (age ࣙ 18 years) that > 140 mmHg or < 90 mmHg, and other changes such
were admitted in the trauma ICU and required mechanical as hypothermia and tachypnea). Data were not collected
ventilation from March 1, 2018, to November 15, 2018. during extracorporeal membrane oxygenation, when there
The requirement to obtain informed consent was waived. was a chest-tube air leak > 10% of tidal volume, when
Patients were excluded if they were transferred from other the patients were being ventilated with FiO2 > 60%, when
institutions, pregnant, or prisoners. the patients were on intermittent hemodialysis (iHD), and
IC was initiated as soon as possible within 4 days of ICU for 4 hours after iHD. However, during continuous renal
admission. We used CARESCAPE R-860 ventilators (GE replacement therapy, REE data were normally collected.
Healthcare, Madison, WI, USA) that have the ability to Data were recorded for up to 14 consecutive days or until
record continuous IC measurements using a gas-sampling transfer out from the ICU, extubation, or death, whichever
module, E-sCOVX or E-COVX (GE Healthcare/Datex- occurred first. Per the manufacturer’s suggestion, the gas
Ohmeda, Helsinki, Finland). Data collected included de- modules were calibrated every 3 months because of their
mographics (age, sex, weight, body mass index [BMI], and use for research purposes.
baseline nutrition status as documented by the registered Based upon parametric or nonparametric distribution,
dietitian [RD]), injury characteristics (injury mechanism, the mean ± SD or median (interquartile range) was re-
underlying injuries, Acute Physiology and Chronic Health ported, respectively. Statistical tests were performed using
Evaluation [APACHE] II score, and surgery within 24 hours Stata for Windows, Version 14.0 (StataCorp LLC, College
and after 24 hours), medications, ventilator settings, labo- Station, TX, USA).
ratory values, and energy/protein prescription and delivery.
There is 1 full-time RD assigned to the trauma ICU, and the
vast majority of initial nutrition assessments and follow-up
Results
assessments were performed by that 1 RD. As recommended Fifty-five patients were included in the final analysis. The
by American Society for Parenteral and Enteral Nutrition median age was 38 [27–58] years, 38 (69%) were male, BMI
(ASPEN), the RD used measurements from the IC to guide was 28 [25–33] kg/m2 , and APACHE II score was 17 [14–
energy prescriptions if those measurements were confirmed 24]. The most common mechanism of injury was blunt
to be taken at steady state and were relatively consistent (n = 38, 69%), followed by penetrating (n = 9, 16%) and
within a single day. However, in times when large variations burn (n = 8, 15%) (Table 1).
were apparent, the RD reverted to using the formula of Measurements were initiated a median of 1 [0–1] day
25–30 kcal/kg. Propofol is commonly used in our ICU for following ICU admission. On day 1 of measurements,
Vasileiou et al 891

Table 1. Patients’ Demographics and Clinical Characteristics. common “finding” was that no corresponding clinical event
was identified.
Patients’ Characteristics N = 55

Age [IQR] 38 [27–58] Discussion


Male (%) 38 (69)
BMI [IQR] 28 [25–33] Based on continuous IC measurements, we report that the
APACHE II [IQR] 17 [14–24] REE fluctuates widely during the first few days following
ISS 26 [17–34] injury in trauma ICU patients requiring mechanical ven-
Mechanism of injury (%) tilation. We defined daily REE variability as [(REEmax −
• Blunt 38 (69) REEmin/2)/average REE], and it is apparent that within
• Penetrating 9 (16) a 24-hour period, 1 single measurement of REE during
• Burn 8 (15)
steady state might not represent a patient’s average daily
ICU LOS [IQR] 21 [10–44]
Hospital LOS [IQR] 31 [16–59] metabolic status or energy needs during the first 14 days.
Ventilator days [IQR] 19 [6–37] At the end of the 14-day period, there were 12 males and
28 ventilator-free days [IQR] 4 [0–22] 5 females remaining intubated, a similar male-to-female
Hospital mortality (%) 9 (16) ratio as on the first day of measurements. Therefore, it
is unlikely that the changes in the recorded median REE
APACHE II, Acute Physiology and Chronic Health Evaluation II;
values can be attributed to more males finishing the 14-day
BMI, body mass index; ICU, intensive care unit; IQR, interquartile
range; ISS, injury severity score; LOS, length of stay. study period. All of our measurements were values recorded
from 10-minute intervals with ࣘ5% coefficient of variation,
the group median for the daily average REE was 1,663 which is a stricter measure of steady state than the one
[1,435–2,143] kcal, and by the seventh day, it had increased that McClave et al suggested (<10% coefficient of variation
to 2,080 [1,701–2,336] kcal, a 25% increase, which was for 5 minutes).10 The 2016 ASPEN/Society of Critical Care
relatively sustained through the 14th day (Figure 1). For Medicine guidelines recommend IC measurements twice a
every day of the 14-day period, the clinical events associated week, when available. Our data suggest that this might not
with the recorded REE maximum and REE minimum are be sufficiently accurate, especially on the first days following
shown on Tables 2 and 3. The calculated REE variability trauma, when variability can be increased, and various
ranged between 8% and 13% (Figure 2). In particular, with steady-state measurements can vary widely.
the exception of the first day of measurements, variability Previous studies have demonstrated the effect that many
was measured to be ࣙ10% for the rest of the days. Tables 2 factors have on a patient’s REE, and consequently, these
and 3 show that there are some clinical events that can daily variations in the clinical picture will affect the average
elevate or reduce REE without affecting the steady state. REE, as evidenced by the calculated REE variability.13-15
However, for every REE minimum and nearly every REE Although the numbers are small, we noted that occa-
maximum in the first 14 days of measurements, the most sionally the maximum REE value was recorded at times

Figure 1. Average REE in the early post-injury period. REE, resting energy expenditure. [Correction added on July 10, 2020 after
first online publication: the axis labeling in the figure was modified.]
892 Journal of Parenteral and Enteral Nutrition 44(5)

Table 2. Clinical Events in the First Week of Measurements.

Day 1 Day 2 Day 3 Day 4 Day 5 Day 6 Day 7


(N = 55) (N = 55) (N = 53) (N = 42) (N = 36) (N = 34) (N = 32)

Clinical events during the recorded REE maximuma


No changes (%) 25 (45) 22 (40) 21 (40) 14 (33) 10 (28) 13 (38) 12 (50)
Fever (T > 38.5°C) (%) 8 (15) 9 (16) 9 (17) 7 (17) 6 (17) 5 (15) 7 (22)
ICP > 15 mmHg (%) 5 (9) 5 (9) 5 (9) 5 (12) 4 (11) 1 (3) 1 (3)
Tachycardia (HR > 120) (%) 12 (22) 13 (24) 14 (26) 7 (17) 5 (14) 6 (18) 4 (13)
Hypertension (SBP > 140 mmHg) (%) 15 (27) 16 (29) 13 (25) 18 (43) 16 (44) 12 (35) 13 (41)
Hypotension (SBP < 90 mmHg) (%) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0) 1 (3) 0 (0)
Other (%) 1 (2) 1 (2) 2 (4) 5 (12) 2 (6) 2 (6) 1 (3)
Clinical events during the recorded REE minimuma
No changes (%) 31 (56) 28 (51) 30 (57) 19 (45) 16 (44) 18 (53) 19 (59)
Fever (T > 38.5°C) (%) 6 (11) 6 (11) 4 (8) 4 (10) 3 (8) 4 (12) 3 (9)
ICP > 15 mmHg (%) 3 (5) 5 (9) 4 (8) 5 (12) 3 (8) 1 (3) 1 (3)
Tachycardia (HR > 120) (%) 9 (16) 7 (13) 4 (8) 4 (10) 2 (6) 2 (6) 2 (6)
Hypertension (SBP > 140 mmHg) (%) 12 (22) 11 (20) 9 (17) 14 (33) 12 (33) 9 (26) 10 (31)
Hypotension (SBP < 90 mmHg) (%) 0 (0) 1 (2) 1 (2) 1 (2) 0 (0) 1 (3) 1 (3)
Other (%) 1 (2) 3 (5) 9 (17) 5 (12) 4 (11) 2 (6) 1 (3)

HR, heart rate; ICP, intracranial pressure; REE, resting energy expenditure; SBP, systolic blood pressure; T, temperature.
a Percentages add up to >100% because multiple clinical events could have been recorded simultaneously.

Table 3. Clinical Events in the Second Week of Measurements.

Day 8 Day 9 Day 10 Day 11 Day 12 Day 13 Day 14


(N = 29) (N = 27) (N = 25) (N = 23) (N = 20) (N = 19) (N = 17)

Clinical events during the recorded REE maximuma


No changes (%) 13 (45) 15 (56) 14 (56) 12 (52) 11 (55) 11 (58) 6 (35)
Fever (T > 38.5°C) (%) 7 (24) 4 (15) 3 (12) 1 (4) 1 (5) 2 (11) 3 (18)
ICP > 15 mmHg (%) 1 (3) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0)
Tachycardia (HR > 120) (%) 4 (14) 3 (11) 2 (8) 6 (26) 5 (25) 2 (11) 1 (6)
Hypertension (SBP > 140 mmHg) (%) 8 (28) 7 (26) 7 (28) 6 (26) 7 (35) 6 (32) 6 (35)
Hypotension (SBP < 90 mmHg) (%) 0 (0) 1 (4) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0)
Other (%) 1 (3) 1 (4) 1 (4) 1 (4) 0 (0) 0 (0) 2 (12)
Clinical events during the recorded REE minimuma
No changes (%) 19 (66) 19 (70) 16 (64) 16 (70) 13 (65) 14 (74) 9 (53)
Fever (T > 38.5°C) (%) 2 (7) 1 (4) 1 (4) 1 (4) 0 (0) 2 (11) 3 (18)
ICP > 15 mmHg (%) 1 (3) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0)
Tachycardia (HR > 120) (%) 1 (3) 2 (7) 3 (12) 3 (13) 1 (5) 1 (5) 2 (12)
Hypertension (SBP > 140 mmHg) (%) 3 (10) 3 (11) 5 (20) 4 (17) 4 (20) 1 (5) 3 (18)
Hypotension (SBP < 90 mmHg) (%) 1 (3) 2 (7) 1 (4) 0 (0) 0 (0) 0 (0) 0 (0)
Other (%) 2 (7) 1 (4) 1 (4) 0 (0) 2 (10) 1 (5) 1 (6)

HR, heart rate; ICP, intracranial pressure; REE, resting energy expenditure; SBP, systolic blood pressure; T, temperature.
a Percentages add up to >100% because multiple clinical events could have been recorded simultaneously.

when clinical events that are expected to elevate metabolic the differences in TEE between days were not significant,
requirements occurred, such as fever, elevated BP, and although they argued that in the individual patient, this
tachycardia. Similarly, at times when the minimum REE was variability may become significant. However, this study was
recorded, events expected to decrease REE were noted, such limited by its wide range of days when measurements were
as reduced BP or hypothermia, which was the most common initiated and by the small amount of patients that completed
event reported as “other.” However, for both REE minimum 7 days of measurements. They initiated measurements on
and REE maximum, the most common “finding” was no day 6 of ICU admission, and less than half of their patients
corresponding clinical event. had measurements for >3 days. When comparing their
Vermeij et al studied the day-to-day variability of TEE in results with our findings, the biggest increase in the daily
critically ill surgical patients.7 In that study, they found that average REE that we measured was within the first 7 days
Vasileiou et al 893

Figure 2. REE variability in the early post-injury period. REE variability = [(REEmax − REEmin/2)/average REE]. REE, resting
energy expenditure. [Correction added on July 10, 2020 after first online publication: the axis labeling in the figure was modified.]

of measurements, when REE rose from a median 1,663 to did not account exactly for the amount of propofol energy,
2,080 kcal, a 20% increase during early hospitalization days. as this is accounted for by the ICU dietitian when adjusting
In our study, no measurements were initiated after 4 days the energy target. Because this was a purely observational
of ICU admission, since we were interested in capturing the study, we did not wish to disrupt the usual practice of the
early postinjury energy requirements and their progress over ICU clinicians. Although this may have led to some impre-
time. Thus, day-to-day variability can change significantly, cision in the calculation of the energy deficits, we believe this
especially in the early days post injury. is a small margin of error, as it is commonly interrupted
for reasons including frequent neurologic examinations in
brain-injured patients, return trips to the operating room,
hypotension, or bradycardia. Another potential limitation
Limitations
of our study is that we did not specifically document every
The study has several limitations that need to be addressed. single ventilator setting change, though we did record the
First, we included only 55 patients, a relatively small sample ventilator settings at the start of each day. It is possible that a
size, precluding strong conclusions. External replication measurement taken shortly after a ventilator setting change
by others would strengthen our conclusions. Additionally, may be inaccurate, though it should be emphasized that all
the exclusion of all patients other than injured patients REE recordings entered into the database were taken during
decreases the generalizability of this study. It would be a 10-minute period of steady state, with <5% variation in
interesting to see whether the increased variability of REE VCO2 and VO2 . Additionally, we did not specifically record
can be seen in other patient populations as well, but this was every single change in the tube feeding rate, and it is possible
beyond the scope of this study. Raurich et al attempted to that changes in continuous feeding may affect the metabolic
describe the differences of REE in various types of lesions, rate. However, a recent study suggests that the thermic effect
including trauma, but failed to identify differences between of food is negligible in an ICU setting when patients are re-
medical, surgical, and trauma patients. However, that study ceiving continuous tube feeding.17 Despite these limitations,
was limited by its retrospective nature and the wide range this study provides meaningful insight into the progression
of days within which the measurements were obtained.16 of REE in critically injured patients during the first 2 weeks
Second, despite our efforts to collect continuous 24-hour of recovery and confirms that, on average, the hyperme-
data, there were sometimes interruptions, some of them tabolic state is sustained, though individual variability can
avoidable. For instance, in many patients, following a neb- be high. Although many consider IC to be the gold standard
ulizer treatment, the nebulizer mode was left on for several for determining the metabolic requirements in critically ill
hours, and the ventilator would not collect IC data until patients, we report that a solitary measurement or sparse
the nebulizer was manually switched off, and then IC mea- measurements may not be accurate. We recommend that
surements could resume. Despite these sporadic, random steady-state measurements be examined at least daily in
interruptions, in most patients we were still able to collect the first 14 days after injury and even more frequently, if
multiple data points throughout each study day. Third, we feasible.
894 Journal of Parenteral and Enteral Nutrition 44(5)

Conclusion 4. Bruder N, Lassegue D, Pelissier D, Graziani N, François G. Energy


expenditure and withdrawal of sedation in severe head-injured patients.
In critically ill injured patients, intermittent REE measure- Crit Care Med. 1994;22(7):1114-1119.
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fluctuation over a 24-hour period and demonstrate a grad- GY. Relative association of fever and injury with hypermetabolism in
critically ill patients. Injury. 1997;28(9-10):617-621.
ual rise over the first few days after injury. Various clinical 6. Swinamer DL, Phang PT, Jones RL, Grace M, King EG. Twenty-
events may be associated with those fluctuations and are not four hour energy expenditure in critically ill patients. Crit Care Med.
necessarily predictive of higher or lower metabolic require- 1987;15(7):637-643.
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reflect the true metabolic requirements (especially during variability of energy expenditure in critically ill surgical patients. Crit
Care Med. 1989;17(7):623-626.
early hospitalization), and continuous REE measurements, 8. Zijlstra N, ten Dam SM, Hulshof PJ, Ram C, Hiemstra G, de Roos
if available, are recommended for capturing the variations NM. 24-Hour indirect calorimetry in mechanically ventilated critically
of metabolism as they occur on a day-to-day basis and their ill patients. Nutr Clin Pract. 2007;22(2):250-255.
relation to patients’ clinical course. 9. Smyrnios NA, Curley FJ, Shaker KG. Accuracy of 30-minute indi-
rect calorimetry studies in predicting 24-hour energy expenditure in
mechanically ventilated, critically ill patients. JPEN J Parenter Enteral
Statement of Authorship Nutr. 1997;21(3):168-174.
G. Vasileiou and D. D. Yeh equally contributed to the con- 10. McClave SA, Spain DA, Skolnick JL, et al. Achievement of steady
ception and design of the research; P. Byers contributed to state optimizes results when performing indirect calorimetry. JPEN J
the design of the research; G. Vasileiou, M. B. Mulder, S. Parenter Enteral Nutr. 2003;27(1):16-20.
Qian, R. Iyengar, and L. M. Gass contributed to the acqui- 11. Monk DN, Plank LD, Franch-Arcas G, Finn PJ, Streat SJ, Hill GL. Se-
quential changes in the metabolic response in critically injured patients
sition and analysis of the data; G. Vasileiou, D. D. Yeh, P.
during the first 25 days after blunt trauma. Ann Surg. 1996;223(4):395-
Byers, E. Lineen, and J. Parks contributed to the interpre- 405.
tation of the data; and G. Vasileiou and D. D. Yeh drafted 12. Plank LD, Connolly AB, Hill GL. Sequential changes in the metabolic
the manuscript. All authors critically revised the manuscript, response in severely septic patients during the first 23 days after the
agree to be fully accountable for ensuring the integrity and onset of peritonitis. Ann Surg. 1998;228(2):146-158.
accuracy of the work, and read and approved the final 13. Bruder N, Raynal M, Pellissier D, Courtinat C, François G. Influence
manuscript. of body temperature, with or without sedation, on energy expenditure
in severe head-injured patients. Crit Care Med. 1998;26(3):568-572.
14. Boulanger BR, Nayman R, McLean RF, Phillips E, Rizoli SB. What
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