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Nutrition in Clinical Practice
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Techniques and Procedures

Monitoring Energy Metabolism with Indirect Calorimetry: Instruments, Interpretation, and Clinical Application

Kalman E. Holdy, MD

Nutrition and Metabolic Support Service, Sharp Memorial Hospital, San Diego, California

Correspondence: Kalman E. Holdy, MD, 7920 First Street, Suite 101, San Diego, CA 92123. Electronic mail may be sent to kalman.holdy{at}sharp.com.

Indirect calorimetry is the best measure to guide calorie administration during nutrition support. This article presents an update of the types of currently available indirect calorimeters and reviews the recent advances that guide the clinical application of indirect calorimetry. The emphasis of this report is placed on issues that the practicing clinician can use to evaluate, interpret, and apply measurements of energy expenditure.

Supporting energy metabolism is an integral part of nutrition support, yet energy expenditure (EE) is infrequently measured. The limitations of equations are predictive well recognized.1–6 Measured resting EE (MREE) obtained from indirect calorimetry (IC) is the best guide to energy administration during nutrition support.1,7 Although IC was a rather standard instrument in many hospitals through the early 1950s, today it is available at far too few institutions and thus is underused in patient care. Because little or no experience with IC is provided during medical education, the benefits of IC are poorly appreciated. New technology, less expense, and a better understanding of how to interpret measurements should lead to more frequent use of IC. This review will compare types of current IC instruments, describe new approaches to the interpretation of MREE, discuss the clinical application of IC, and reevaluate energy metabolism in terms of body composition, cellular, and organ EE.


   Categorization of Current IC Instruments
Top
 Categorization of Current IC...
Changes in Interpretation
 Clinical Application
 Body Composition and EE...
 Summary
 
For routine clinical use, there are 3 broad categories of instruments that measure EE: the "classic" metabolic cart, new portable hand-held instruments, and more recently developed armband sensors (Table 1). An additional technique, circulatory IC, estimates EE from the Fick equation after measuring cardiac output. Circulatory IC correlates with respiratory IC across large groups of patients, but accuracy is poor in a specific patient. Variation in an individual patient between the 2 techniques (classic respiratory vs circulatory IC) reaches 50%.8 Therefore, circulatory IC is much less applicable to individual patient care.1,8


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  		Table 1 Comparison of indirect calorimetry instruments available in clinical practice

 

"Classic" Metabolic Carts
"Classic" respiratory metabolic carts measure oxygen consumption (VO2) and carbon dioxide production (VCO2) and automatically calculate EE, along with the respiratory quotient (RQ).7 These instruments are portable, yet somewhat bulky. They can be used both with mechanically ventilated patients and those spontaneously breathing room air. "Classic" metabolic carts represent the technology used to derive most modern predicative equations in a range of subjects from normal healthy volunteers to critically ill patients. Respiratory therapists are usually required to operate the "classic" cart because these instruments must be calibrated before each test and expertise related to pulmonary function testing and the circuitry of mechanical ventilators is important.7,9

A common concern among clinicians and hospital administrators is the expense and the staffing that is required to conduct IC.10 Although the cost is high (Table 1), it is similar to the purchase price of modern, complex beds typically used in intensive care units (ICUs). The "purchase price" of a metabolic cart in perspective correlates to about $12 per test, if an average of 200 tests is performed per year over 10 years. The expertise required to conduct IC is similar to the requirements for other common hospital tests, such as echocardiograms. In our experience, the respiratory therapy department can incorporate IC into the therapists' work schedule with minimal to no additional personnel. Typically, a metabolic cart study takes about 30 minutes of test time (plus setup time) to yield a valid MREE.7 Longer test times or even continuous IC may be needed if a steady state cannot be achieved within 30 minutes (see Test Validation below).

Continuous IC monitoring is difficult with the metabolic carts currently available for purchase in the United States. Modular units for continuous monitoring, which are attached to ventilators or are part of bedside monitoring units, are currently unavailable in the United States (previous models were either discontinued or were found to be incompatible with more recent ICU instrumentation). Evaluation of new continuous IC monitors is in progress. A good substitute for continuous IC is the combination of 4 15-minute measurements equally spaced throughout the day.11

Small Highly Portable IC Devices
New IC devices, which measure only VO2, have recently become available for clinical application (Table 1). These instruments are much more compact and thus are much more highly portable than the "classic" metabolic cart. One such device is a small handheld unit that can easily be carried in transport from one subject to the next. Because only VO2 is measured, no RQ is determined. These instruments are self-calibrating and need minimal operator training for proficient testing. The test time is approximately 10 minutes. The handheld unit weighs only 4 oz. It provides a VO2 value and MREE on its liquid crystal window display. Several independent validation studies of the handheld unit have recently appeared.12–14 Published experience with this unit has been in ambulatory healthy individuals. The less portable "hybrid" unit weighs about 5 pounds and requires a printer to generate a report. Validation of this latter instrument is limited to the "white paper" posted on the website (Table 1). No validation has yet been published in critically ill patients with either of these instruments. These units cannot be used with patients requiring mechanical ventilation or those in whom supplemental oxygen cannot be temporarily discontinued. The purchase price of these portable calorimeters is about one-tenth of the cost of a "classic" metabolic cart. The ease of use and lower purchase price of these smaller highly portable units brings IC within reach of many nutrition specialists and healthcare providers.

New Armband Sensors
A new technique to measure EE involves heat flux sensors mounted on a small armband (Table 1). The values obtained by these instruments approximate those made by direct calorimetry because heat flux is the primary physiologic parameter being measured (as opposed to respiratory gas exchange by "classic" IC instruments). The armband sensors are being used in the ambulatory setting for lifestyle modification such as weight management, fitness improvement, and diabetes care. Although this technology is intriguing, validation is limited and available only for ambulatory patients. No evaluation of the armbands is available in critically ill or hospitalized patients.


   Changes in Interpretation
Top
 Categorization of Current IC...
 Changes in Interpretation
Clinical Application
 Body Composition and EE...
 Summary
 
Interpretation of IC measurement has advanced regarding test validation, application of the RQ, and adjustment of the MREE with activity or stress factors (Tables 2 and 3).


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  		Table 2 Validation of a metabolic cart study*

 

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  		Table 3 Indirect Calorimetry (IC) application*

 

Test Validation
Before applying data obtained from a "classic" metabolic cart, the validity of the measurements must be verified by at least 2 essential parameters: evaluation of the RQ and documentation that steady state has been achieved (Table 2).7,9 The RQ should be within the physiologic range of 0.67 to 1.3. Approximately 5% to 8% of ventilated or ambulatory patients tested with a "classic" metabolic cart have an RQ outside of the physiologic limit, thus invalidating the test.15,16 A valid test requires a "steady-state" period of gas exchange, defined by a 5-minute interval during which VO2 and VCO2 vary by ≤10%.7 The importance of achieving a steady-state time interval to validate measurements from short-term "snapshot IC" has been reexamined.16,17 McClave et al17 recently determined in mechanically ventilated patients that a 5-minute steady state defined by the most stringent criteria (VO2, VCO2 vary by <10%) best represents the measured 24-hour total EE (TEE; R = 0.942 to 0.960). Several other less stringent criteria (VO2, VCO2 vary by >10%) to define the steady state correlate less well with TEE.17 In healthy volunteers or ambulatory chronically ill patients, Reeves et al16 recently reported that a steady state as short as 3 minutes reflects a clinically acceptable MREE. Steady state can generally be achieved within a test time of 30 minutes. However, if a steady state interval of sufficient time (5 minutes in critically ill mechanically ventilated patients and 3 minutes in ambulatory patients) cannot be obtained within 30 minutes, the measurement time may have to be extended. The time extension should be dictated by the coefficient of variation (a statistical measurement of variation in the minute-by-minute average values for VO2 and VCO2; Table 2).7,17 A variety of additional technical factors need to be considered to ensure accurate IC testing.7,9

The instruments that measure only VO2 (Table 1) determine the steady state and calculate the REE using a constant arbitrary value for RQ. The error to the MREE introduced with a fixed RQ of 0.85, without a VCO2 measurement, is <4% (Fig. 1). The MREE with these instruments accurately reflects REE and may be applied in the same manner (Table 3) as the MREE measured by a "classic" metabolic cart.


Figure 1
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  		Figure 1. Variation of the REE with the RQ and the error introduced by neglecting to measure the VCO2. The variation of EE at 3 VO2 levels is calculated using the Weir equation,49 EE = 3.94 x VO2 + 1.11 x VCO2. Within the RQ range of 0.70 to 1.0 (shaded area), assuming a fixed RQ of 0.85, measuring only the VO2 introduces <4% error to the MREE. If a patient's actual RQ is 0.85 to 1.0, neglecting the VCO2 results in an underestimation of the REE (–48 kcal/d to –71 kcal/d, over the VO2 range considered). If a patient's actual RQ is 0.70 to 0.85, neglecting the VCO2 results in small overestimation of the REE (+48 kcal/d to +71 kcal/d, over the VO2 range considered).

 

Interpreting the RQ
Recent studies evaluating the clinical utility of the RQ have shown that its usefulness is limited to study validation.15 The common use of the RQ to adjust and guide energy provision or adjust macronutrient composition7,9 is not supported by these studies for current clinical practice.15 An RQ of 0.85 is generally considered or expected to indicate appropriate energy provision in a patient on a mixed-fuel regimen (such as a standard enteral formula provided at a volume which meets caloric requirements). However, variation of the RQ above or below 0.85 does not reliably predict over- or underfeeding (Fig. 2). McClave et al15 found that in 263 patients, about 8% of patients who were underfed (receiving <90% of caloric requirements) had an RQ >1.0 and about 28% of patients who were overfed (receiving >110% of requirements) had an RQ <0.85. The RQ correlated with the degree of feeding in the entire study group (Fig. 2) but was not patient specific. A rise in the RQ in response to nutrition support may indicate tolerance limits (elevations in RQ >1.0 correlated significantly with development of shallow, rapid respirations, suggesting intolerance).15,18 Therefore, the RQ should be used to confirm that the IC study is physiologic and without artifactual error. The RQ should not be used to adjust macronutrient composition or infer appropriateness of energy provision.17


Figure 2
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  		Figure 2. The measured RQ and the effect of nutrition support. The RQ correlates with the calories fed in the entire group studied (R2 = 0.16, p = .0001). If an RQ of 0.85 to 1.0 is used as the RQ for appropriate feeding, the distribution in sections A-B indicates failure to detect underfeeding and the distribution in sections C-D indicates failure to detect overfeeding. The marked variability of the relationship of the RQ to feeding precludes applying the RQ to adjust patient-specific nutrition support. Adapted from reference 15 with permission from the American Society for Parenteral and Enteral Nutrition (A.S.P.E.N.). A.S.P.E.N. does not endorse the use of this material in any form other than its entirety.

 

Adjusting the MREE
The adjustment of MREE to better estimate TEE has changed significantly over the last 2 decades.3,5,17 EE during hospitalization has decreased since the early years of modern nutrition support.5 The decrease can be explained by a variety of advances in clinical care.5,2 Recently the metabolic activity factors, used to adjust the value for resting EE (REE) obtained from predictive equations in critically ill patients, have been reevaluated.3 The MREE does eliminate the need for such metabolic activity or "stress" factors because the measured value accurately reflects TEE (which incorporates the increases in REE caused by metabolic stress). The use of a small 10% activity factor in critically ill, mechanically ventilated patients (to reflect the added EE related to routine nursing care in the ICU) has been common practice.7 Recent careful evaluation of this practice indicates that in the modern ICU, the MREE of ventilated patients equates TEE without any multiplication factors.2,17 to For example, McClave et al17 showed that the MREE, determined after achieving steady state during IC, accurately reflects the total 24-hour TEE, without any correction factors. Adding a 10% activity factor decreases the accuracy with which a short-term "snapshot" IC measurement of REE correlates to measured 24-hour TEE. The previous recommendations for estimating TEE in ventilated ICU patients required adjustment of the MREE by an activity factor to account for short bursts of EE related to nursing care during ICU care. This practice is no longer warranted and should be abandoned.5,17 Therefore, in mechanically ventilated patients no adjustment of MREE is needed as long as steady state is achieved during IC. In spontaneously breathing patients, MREE should be increased in proportion to activity to estimate TEE.18–21 This adjustment is largely empiric, ranging from 10% to >75% (Table 3).

The adjustment of MREE obtained during fever has not been studied.22 Although studies in the past have shown that EE increases 7% for each degree Fahrenheit above 100°,7 it does not necessarily follow that a "afebrile REE" should be estimated from a MREE obtained in a patient during fever. Such practice, similar to adding arbitrary activity factors as described above, may introduce artifactual error and reduce accuracy in the critically ill patient. One reasonable approach, until more data are available, is to remeasure such patients when they are afebrile or adjust the measurement obtained during the febrile episode after the fever resolves.


   Clinical Application
Top
 Categorization of Current IC...
 Changes in Interpretation
 Clinical Application
Body Composition and EE...
 Summary
 
IC is the best patient-specific guide for macronutrient administration during nutrition support. Wooley and Sax23 recently provided a "primer" regarding the application of IC to patient care with excellent case examples. A major challenge in the formulation of a nutrition support regimen is to estimate the metabolically active weight (feeding weight) for use in predictive equations.24,25 The feeding weight is most uncertain in cachectic and obese patients. Employing IC in these situations eliminates this uncertainty. IC influences nutrition support (Table 4). Three recent studies show that nutrition support is altered in about 50% of patients following IC.18,26,27 The application of IC appears to influence nutrition support most in ventilated patients and in patients with extremes of body composition (BMI <18 or >30 kg/m2).26,27 These patients are precisely those for whom determining the feeding weight is so difficult. Frequent adjustment of nutrition support based on daily28 or continuous IC monitoring,29,30 although challenging, has been suggested recently. However, even a single evaluation with IC influences feeding and may provide marked cost savings.25


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  		Table 4 How indirect calorimetry influences nutrition support

 

The value obtained by IC is a measure of energy "use" rather than energy "need."31,32 Energy use reflects the exact EE associated with metabolism of nutrient substrate (endogenous and exogenous) at a given point in time, irrespective of tolerance, assimilation, or stress-induced errors of metabolism. Energy need is a more nebulous estimate than energy use, incorporating the MREE with other aspects of nutrition assessment, such as the expected tolerance for macronutrients, errors in the biochemical handling of substrate (such as those factors which lead to hyperglycemia), and whether calories need to be added/subtracted to promote weight gain/loss. MREE is an objective, accurate, patient-specific caloric reference. Energy need, on the other hand, is based on the clinical condition of the patient and on the route of feeding. Nutrition support may be provided at a fraction of the MREE (permissive underfeeding),33–35 at the MREE, or above the MREE (Table 3). In the critically ill patient, the MREE is the energy goal to which enteral nutrition should be targeted. The specification of this target is important for enteral nutrition because provision of calories all too often falls below MREE because of problems with intolerance.10,18,22 Parenteral nutrition in critically ill patients should be limited by the MREE because the ease of IV administration of nutrients often results in overfeeding.10,17,22

Underfeeding is permissible for a finite period of time that is yet to be determined. Monitoring cumulative energy balance may evolve as a tool to determine a "threshold" value of caloric deficit which signals the need for additional nutrition support. A negative cumulative energy balance has been shown to correlate with adverse outcome.28,36–39 However, the impact of nutrition support intervention in chronic critical illness, according to IC and cumulative energy balance, has yet to be studied. Whether nutrition therapy that maintains a positive cumulative energy balance can influence ICU outcome, hospital length of stay, and long-term functional recovery in chronic critical illness requires further evaluation.

The application of the highly portable, inexpensive IC devices (those which measure only VO2) to nutrition support is evolving.40 These instruments, and the armband sensors, may eventually become useful guides for home long-term nutrition support. Weight gain in such patients over brief periods of time results in deposition of adipose tissue with little gain in lean body mass.21 Energy provision based on IC with the these new techniques may refine nutrition support to optimize changes in body composition. These new instruments provide exciting tools for research and patient care.


   Body Composition and EE of Specific Organ Systems
Top
 Categorization of Current IC...
 Changes in Interpretation
 Clinical Application
 Body Composition and EE...
Summary
 
TEE is the sum of several measured components: the REE, the EE associated with physical activity, and the EE related to the thermogenesis of food. IC generally measures that component which comprises the REE. However, the EE expressed for each of the above components consists of similar metabolic processes, altered in proportion to specific cellular and organ systems.41–43 For example, similar cellular processes utilize energy in the heart and skeletal muscles at rest and during exercise,41 but quantitatively their contributions to REE are very different. Therefore, an alternative consideration in understanding whole body metabolism is to consider EE in terms of body composition and the individual contributions from specific organ systems in health and disease.41,44 Organ-specific EE in healthy individuals, when measured, was found to evolve with age.41 The closer correlation of EE to lean body mass rather than total body mass (or actual body weight) is well recognized.19 With several new techniques, organ-specific EE can be measured in healthy volunteers and even critically ill patients (such as burn patients).44,45 About 90% of the total change in REE in burn patients can be related to changes in EE related to specific organ systems. About 60% of this is accounted for by ATP-related changes in metabolism.44

Maintaining body composition that optimizes function is an important goal of nutrition support.46 It follows that considering EE in terms of body composition is necessary to promote advances in nutrition support.47 This is illustrated in the recent finding that critically ill, cachectic patients have a per kilogram EE higher than similar patients of normal weight.47 A likely explanation centers on the alteration in body composition of cachectic patients. The metabolically active internal organs of the cachectic patient represent a much larger fraction of the total body weight compared with patients with more normal body composition.47,48


   Summary
Top
 Categorization of Current IC...
 Changes in Interpretation
 Clinical Application
 Body Composition and EE...
 Summary
 
The "classic" metabolic carts (which measure both VO2 and VCO2) are the "workhorse" instruments that may be applied across a wide range of hospitalized to nonhospitalized and acute to chronic patient populations. IC should be performed with the same expertise as other hospital-based testing, such as standard pulmonary function tests. Interpretation of IC requires evaluation of test validity using the RQ and steady state gas exchange. Poor reliability in the RQ prevents its use in determining rate of caloric provision or nature of macronutrient composition. The MREE, without correction factors, is the simplest, best guide to determine TEE and direct nutrition support goals for mechanically ventilated ICU patients. New, less expensive, highly portable indirect calorimeters, which measure only VO2, accurately determine REE and are applicable to ambulatory patients. These latter instruments may also become more useful in hospitalized, nonmechanically ventilated patients. Understanding energy metabolism at the organ level is a new, exciting, and evolving dimension of energy metabolism.

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Nutrition in Clinical Practice, Vol. 19, No. 5, 447-454 (2004)
DOI: 10.1177/0115426504019005447
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