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April 2009 Issue

A Guide to Indirect Calorimetry
By Ashley Doyle-Lucas and Brenda M. Davy, PhD, RD, FACSM
Today’s Dietitian
Vol. 11 No. 4 P. 50

Suggested CDR Learning Codes: 3000, 3010; Level 3

Indirect calorimetry is the gold standard technique for determining resting energy requirements.1,2 It is of significant interest to dietitians and the third most often searched term by RDs accessing the American Dietetic Association’s online Evidence Analysis Library. This article presents a brief overview of the background and development of this technique, measurement considerations, and an overview of recommended prediction equations for various client populations, including athletes.

Background
Dr. J. Arthur Harris and Francis G. Benedict developed the first two equations for predicting resting energy expenditure (REE), the primary component of total daily energy expenditure (TDEE), in 1919. Today, more than 200 such equations exist, and the accuracy of each in regard to body composition, nutritional status, life span, and ethnicity is still being tested. Open-circuit indirect calorimetry is currently the technique most widely used in laboratory and clinical settings to measure REE and determine the rates of energy utilization and substrate oxidation.3 Significant advancements in this technique of gas exchange measurement within the last 10 years have allowed indirect calorimetry to become more readily available for clinical application. Although commonly considered more accurate than the use of predictive equations for determining REE, indirect calorimetry has potential limitations, which will be presented.3

Measurements from indirect calorimetry are fundamental in clinical and research settings. REE measurements are used in the research areas of obesity, sports nutrition, and aging, as well as in the development of nutritional therapy for individuals with critical illnesses, such as sepsis, burns, organ failure, and cancer.4 These measurements are also used in clinical practice, especially weight management.

Indirect calorimetry is the quantification of REE via measurement of inspired oxygen (VO2) and expired carbon dioxide (VCO2) concentrations.5 Precise measurements of the consumption and production of these gases are used in the Weir equation to calculate REE (kilocalories per day): REE (kcal) = [(VO2 L/min) X 3.941 + (VCO2 L/min) X 1.11] X 1,440 min/day.

The respiratory quotient (RQ) vs. the respiratory exchange ratio, when measured at the mouth, may also be calculated from VCO2 and VO2 via division of the two values (ie, VCO2/VO2).6 RQ is used to determine substrate utilization; an RQ of 0.7 represents lipid metabolism, a value of 0.8 reflects protein metabolism, a value of 0.85 indicates mixed fuel metabolism, and a value of 1 represents pure glucose oxidation. Such physiological RQ ratios may vary from 0.67 (representing ketone body metabolism during fasting) to 1.3 (associated with de novo lipogenesis, hyperventilation, or mechanical ventilation). RQ may also be used to assess test quality and outcomes. If values do not lie within this accepted range and/or are inconsistent with the patient’s nutritional intake, the test should be repeated.3 For example, if the averaged RQ value is less than 0.67, this may signify a leak in the gas collection tube.

Energy Metabolism
Daily energy expenditure may be divided into four primary components3:

• Basal metabolism (~ 60% to 70% of TDEE), which is the energy expended when an individual is supine, in the morning upon waking in a rested, postabsorptive state. Basal energy expenditure, often used interchangeably with REE, includes energy required for the functioning of vital organs, such as the heart, lungs, brain, liver, kidneys, sex organs, muscles, and skin, as well as the energy expended during substrate oxidation and thermoregulation.4,7 Most (83%) of the variance in basal metabolism is explained by fat-free mass (FFM), while the remaining variability may be influenced by age, sex, and genetics.8

• Physical activity (~ 30% or more of TDEE), which is the most variable component of TDEE from one individual to the next.

• Thermic effect of food (~ 5% to 15% of TDEE), which includes the energy necessary for digestion, absorption, and food storage.9

• Nonexercising activity thermogenesis (NEAT), which consists of the energy expended through subconscious movement resulting from occupation.3 The percentage of TDEE attributable to NEAT may range from ~ 6% to 12% and is currently under study as a critical component to TDEE.7

All dietary macronutrients have a common pathway in human metabolism: substrate oxidation to produce energy. These energy-yielding nutrients sustain life through various metabolic reactions via which they are ultimately oxidized to carbon dioxide and water. A fraction of the chemical energy produced through this process (called “free energy”) is captured in high-energy molecules, the most significant being adenosine triphosphate (ATP) and phosphocreatine. The remaining energy produced through oxidation is released as heat, which helps maintain thermoregulation. ATP is associated with a high transfer potential, allowing it to transport the free energy to biochemical processes that require energy for function, such as basal metabolism.

Indirect calorimetry measures oxygen consumption rather than heat production (direct calorimetry). In humans, most heat production originates from oxidative reactions that use oxygen as a reactant. The amount of oxygen used to oxidize the substrates (carbohydrate, protein, fat, alcohol) varies, and the energy yield per mole of oxygen for each has been determined.

Therefore, with these values known (see Table 1), heat production (energy expended) can be calculated from the amount of oxygen consumed.7 For example, VO2 and VCO2 values can be converted into values of energy expenditure (kilocalories per day). As indicated in Table 1, the greatest amount of ATP derived from the three main fuels (glucose, lipid, and protein) is from glucose at 3 moles of ATP per mole of glucose. This illustrates the known concept that carbohydrates have a higher energy yield than lipids or proteins.3 Oxidizing glucose is, therefore, the most efficient process of oxygen utilization for producing energy (ATP); protein and fat oxidation are more costly.6

Instruments and Techniques
Indirect calorimetry is noninvasive, reliable, and relatively easy to perform. There are a variety of instruments available; a major difference among the instruments is in their method of determining VO2, specifically, via an open or closed circuit system.4

Closed-circuit calorimeters were first used by Harris and Benedict in their original experiments, from which they developed the first REE prediction equation.4 Closed-circuit instruments determine VO2 via volumetric changes that are measured from a reservoir of oxygen over a period of time.5 Open-circuit calorimeters, however, are now more commonly used. Open-circuit instruments determine VO2 by measuring the difference of inspired to expired gas concentrations.5 The first open-circuit device of tested accuracy was the Douglas bag method.10 This method required an individual to breathe into a large canvas bag. The gas exchange was then measured and REE was estimated. This method predominated for more than a century.

Modern technology has progressed to computerized systems that measure the expired ventilation rates. These systems have other advanced features, such as portability, automated calibration, and immediate calculations.4 These instruments use various methods for gas analysis and collection, including breath-by-breath technology, mixing chambers, and dilution systems.

• The breath-by-breath system was initially designed for testing in the area of exercise physiology but has been modified for use with patients on ventilators. With this design, air samples are taken on every breath and measurements are averaged at a factory preset time to obtain mixed expired gas values.4,5 One portable device currently available is a handheld instrument called the MedGem by Microlife USA, Inc of Dunedin, Fla., which displays REE (kilocalories per day) and VO2 (milliliters per day).

Eight studies compared the MedGem with four different traditional metabolic carts. In six studies, REE values ranged from 0.1% to 4% compared with the values of the metabolic carts, with an interclass reliability range of 0.76 to 0.92.11 The instrument has been studied in 14 different human trials and, when compared with the measurements of referenced indirect calorimeters, the MedGem proved accurate and reliable for determining REE. However, its use within the healthy older adult population has recently been questioned.12

• Mixing chambers are the most common devices used for determining REE; this system is better designed for steady-state metabolic testing.4 These instruments often use canopies, mouthpieces, or masks to collect gas exchange.13 Expired gas from an individual is directed into the mixing chamber where baffles interrupt flow, prevent streaming of gases, and decrease uneven gas concentrations. At the end of the mixing chamber, a vacuum pump reserves a sample of the mixed expired gas for measurement of expired oxygen and expired carbon dioxide.

Like the breath-by-breath system, the analyzers sample the inspired gas concentrations to determine the differences between inspired and expired gases at factory- or clinician-preselected intervals.4,5 This type of system may be associated with increased error due to potential complications in calibration.

• Dilution systems are flow-generating devices that dilute expired gases with room air and draw gases into a mixing chamber for analysis.4 These systems may also be designed with canopies and can be used to assess nutritional needs in patients who are critically ill.

Currently, there is no gold standard instrument that is recommended to measure energy expenditure. The specific device used should be chosen with regard to its purpose (research, outpatient clinic, adult vs. pediatric patients) while considering cost and ease of use.4 For example, in weight management clinics or outpatient care, the less expensive handheld devices may be most appropriate.5 Despite the instrument used, the technique of the technician measuring energy expenditure through indirect calorimetry must be precise.

Methodological Considerations
Instrument and investigator error and biological variability in energy expenditure measurements must be minimized to accurately determine REE.9 The technician should employ good practices, as the proper running of indirect calorimeters requires technical training, frequent cleaning of the machine, and accurate calibration prior to each test.4,9 Many machines need to be turned on for a specific period of time prior to the test—30 minutes is common—to warm up the dilution pump.

Biological variability is difficult to control due to the myriad factors that influence energy expenditure. For example, anxiety (possibly due to unfamiliarity with the machine and laboratory environment), stresses, diurnal variation, prior physical activity, fidgeting, energy intake, sleep, and medication usages may all affect resting metabolic rate.9 To improve the accuracy of indirect calorimetry, the test should be performed prior to the onset of daily activities while the individual is in a rested state. If the individual has traveled to the testing site, he or she should rest supine for approximately 20 to 30 minutes prior to testing to avoid the effects of voluntary physical activity. The testing environment should be quiet, thermoneutral, and darkly lit; interactions with the technician should be minimized; and the testee should remain awake but restful with minimal movement.

The individual undergoing indirect calorimetry should be advised to avoid strenuous physical activity for a minimum of 14 hours prior to the day of the test and moderate physical activity for at least two hours. The individual should fast for at least six hours, avoid caffeine consumption and medication usage (if possible) overnight, and abstain from nicotine for a minimum of two hours prior to the test.14

It has been reported that a single measurement in healthy adults is sufficient to ensure accuracy (if the results are within the physiological range for RQ and a steady state has been achieved for five minutes). However, the optimal measurement duration remains to be determined.14 An averaged interval after the individual reaches a steady state (ie, a period of five to 15 consecutive minutes in which variations of VO2 and VCO2 are less than 10%) is often suggested. Total test duration may range from 20 to 45 minutes, and studies report small mean differences in REE between various length tests.15,16 During the test, the technician should monitor the equipment and the individual being tested.

Factors Influencing Measurements
• Energy intake: The thermic effect of food acutely increases REE measurements dramatically, more so than physical activity, caffeine consumption, or nicotine ingestion.17 In nonobese adults over a five- to six-hour fast after eating, 7% to 9% of total calories consumed are expended via the thermic effect of food. The peak thermic effect of food occurs within 60 to 180 minutes following a meal.18 As an example, the ingestion of 500 kilocalories increases REE by 17% for four hours following a meal.17 To avoid the effects of the thermic effect of food, a five-hour minimum fast is required before performing indirect calorimetry.18,19

• Timing: REE should be measured in the early morning while the individual is in a quiet, resting (but awake) state; measurements taken in the afternoon are 5% to 6% higher than those taken in the morning.20 However, if testing must be done in the afternoon, it can be assumed that the measurements will be about 100 kilocalories per day higher than morning measurements.21

• Caffeine: The ingestion of caffeine is known to acutely increase metabolic rate. Caffeine ingestion increases REE over baseline in both younger and older populations of men and women, and this increase in REE remained elevated for more than 90 minutes in young men and women.22,23

An overnight fast from caffeine will allow REE values to fall back to baseline in most healthy adults.21 To avoid the effects of caffeine in REE measurements, individuals should refrain from caffeine for four or more hours prior to testing.

• Nicotine: The chronic effects of nicotine on REE have not been determined. However, several studies reported that smoking acutely increased REE by 6% to 12% over a period of 100 to 240 minutes. The dose response of nicotine is unclear. Thus, individuals undergoing testing should avoid nicotine for two hours or more prior to testing.

• Physical activity: The effect of physical activity on REE is dependent on many factors, including duration, intensity, and type of activity performed. A rapid decline in energy expenditure postexercise of varying durations (20 to 80 minutes) and intensities (35% to 68% VO2max) has been reported; however, prolonged elevations in energy expenditure have also been reported following higher intensity exercise (50% to 70% VO2max). Thus, there may be an intensity-duration threshold that must be attained for a prolonged effect on REE.

The overall health and training status of the individual and the type of physical activity performed also affects REE differently. For example, individuals cycling for 30 minutes at 70% of VO2max returned to baseline REE within 80 minutes following the exercise bout. Trained athletes returned to baseline REE more quickly than untrained individuals who cycled at the same intensity and duration. Walking and jogging at a moderate intensity (45% to 65% VO2max) increases REE for a shorter period postexercise; three studies of healthy adults reported that REE returned to baseline within 30 to 60 minutes following 20 to 30 minutes of such exercise. The mean REE measured after 60 to 70 minutes following the exercise was within plus or minus 5% of baseline REE values measured prior to activity.

Resistance training also increases REE, with prolonged effects still detected after 90 minutes of weight lifting. Burleson et al reported that energy expenditure following weight training (resistance exercise) may be greater than that following aerobic exercise when the activities are matched for duration and oxygen consumption.24

Although further research is necessary to pinpoint optimal recovery time to prevent prolonged effects of physical activity in REE measurements, common recommendations are to refrain from long-duration and high-intensity exercise for more than 14 hours prior to indirect calorimetry. If an individual performs more than 30 minutes of low- to moderate-intensity activity, a two-hour recovery period is necessary prior to testing.

• Menstrual cycle: REE fluctuates during the menstrual cycle.9 REE decreases during menstruation (day 1 is the day before menstruation) and throughout the follicular phase (days 15 to 23), with the lowest point occuring one week before ovulation. REE is higher in the luteal phase (days 11 to 14), possibly due to elevated serum concentrations of estrogen and progesterone. REE appears to be relatively stable on days 5, 6, and 7 after the onset of menses.25 Women should be tested during the follicular phase of their cycle, specifically within 10 days after the onset of menses.

• Body composition: FFM is the greatest determinant of REE and contributes significantly to the variation in measurements between individuals. Therefore, adjusting REE for differences in body composition is necessary for comparing energy expenditure between individuals. FFM is comprised of metabolically active viscera that contribute significantly to the total REE of an individual. This includes organs, which are associated with high metabolic rates (200 to 442 kilocalories per kilogram per day) and skeletal muscle and bone mass, which have low metabolic rates (under 14 kilocalories per kilogram per day).

For example, 70% to 80% of REE in a healthy adult is due to the metabolism of the liver, heart, kidneys, and brain, which in total comprise only 7% of actual body weight. Muscle mass in the same individual comprises 88% of organ mass and 44% of FFM but only 28% of the REE.

A decrease in energy expenditure per kilogram body weight accompanies growth and aging. This relationship is due to a slower increase in REE than FFM. In other words, the metabolically active tissue increases less than actual body weight—from the span of ages 20 to 60, there is an average doubling of body fat. Therefore, although associated with a higher REE, a decreased energy expenditure per kilogram body weight will accompany a larger individual, as the smaller individual will have a higher proportion of high metabolically active viscera. The most accurate representation of REE is, therefore, achieved by looking at the energy expenditure per kilogram FFM and the proportional contribution of organs to total body weight.

Comparison With Prediction Equations
There are many REE equations; the most accurate for a given situation may depend on the patient. The Harris-Benedict, Mifflin-St. Jeor, Owen, and Cunningham equations (see Table 2) are examples of those that dietitians widely use to predict REE.

The Harris-Benedict equation is one of the oldest and most commonly used predictive equations. This equation is primarily associated with individual error of overestimation. Frankenfield et al reported that 69% of 136 nonobese male adult REE values predicted with the equation to be within 10% of measured REE.26 Similarly, another study reported that the REE of 80% of tested healthy adults was within 10% of measured; of the remaining individuals, error rate of overestimation was 42% and underestimation was 23%.27 Frankenfield et al concluded the Harris-Benedict equation to overestimate REE by at least 5%, applying most accurately to individuals with a body mass index of 35 to 40.

The Mifflin-St. Jeor equation generally underestimates REE compared with measured values. Frankenfield et al reported that 82% of the REE of healthy adults were estimated within 10% of the measured REE when using the Mifflin-St. Jeor equation.28

The Owen formula may be slightly less accurate as compared with measured REE, with a 28% individual error of overestimation and a 24% error of underestimation in healthy adults.

Frankenfield et al compared REE estimates using the Harris-Benedict, Owen, and Mifflin-St. Jeor equations to measured REE via indirect calorimetry in nonobese, obese, and morbidly obese men. The Mifflin-St. Jeor equation provided the greatest accuracy to measured REE in the nonobese and obese men and was more accurate than both the Harris-Benedict and Owen equations, which were similar to one another.28 The comparison of individual errors in nonobese adults produced by the Owen, Harris-Benedict, and Mifflin-St. Jeor equations are presented in the Evidence Analysis Library. According to the evidence library, the Mifflin-St. Jeor equation is accurate (plus or minus 10% of the measured resting metabolic rate) 82% of the time, with greatest individual errors of underestimation at 18%.

Conclusions
Indirect calorimetry, although commonly accepted as the recommended technique for determining REE, is not without limitations. An understanding of the principles underlying this technique, as well as an awareness of methodological considerations, will assist dietitians with incorporating this procedure into their practice. Measurement errors can be reduced by following standardized, recommended measurement procedures and avoiding situations that may increase variability in testing outcomes. Accurate determination of REE is an integral part of the Nutrition Assessment Process for dietitians in a wide variety of practice settings; it is the basis for estimating daily energy requirements for those with critical illnesses and diabetes, as well as for athletes and individuals seeking weight management medical nutrition therapy.

— Ashley Doyle-Lucas is a doctoral candidate, and Brenda M. Davy, PhD, RD, FACSM, is an associate professor in the department of human nutrition, foods, and exercise at Virginia Tech. Their research is focused on energy balance, eating behaviors, and weight management.

References
1. Boullata J, Williams J, Cottrell F, Hudson L, Compher C. Accurate determination of energy needs in hospitalized patients. J Am Diet Assoc. 2007;107(3):393-401.

2. Schoeller DA. Making indirect calorimetry a gold standard for predicting energy requirements for institutionalized patients. J Am Diet Assoc. 2007;107(3):390-392.

3. Simonson DC, DeFronzo RA. Indirect calorimetry: Methodological and interpretative problems. Am J Physiol. 1990;258(3 Pt 1):E399-412.

4. McClave SA, Snider HL. Use of indirect calorimetry in clinical nutrition. Nutr Clin Pract. 1992;7(5):207-221.

5. Branson RD, Johannigman JA. The measurement of energy expenditure. Nutr Clin Pract. 2004;19(6):622-636.

6. Ferrannini E. The theoretical bases of indirect calorimetry: A review. Metabolism. 1988;37(3):287-301.

7. Martha H. Biochemical, Physiological & Molecular Aspects of Human Nutrition, 2nd ed. New York: Saunders; 2006.

8. Lucas AR, Beard CM, O’Fallon WM, Kurland LT. Anorexia nervosa in Rochester, Minnesota: A 45-year study. Mayo Clin Proc. 1988;63(5):433-442.

9. Donahoo WT, Levine JA, Melanson EL. Variability in energy expenditure and its components. Curr Opin Clin Nutr Metab Care. 2004;7(6):599-605.

10. Bassett DR Jr, Howley ET, Thompson DL, et al. Validity of inspiratory and expiratory methods of measuring gas exchange with a computerized system. J Appl Physiol. 2001;91(1):218-224.

11. McDoniel SO. Systematic review on use of a handheld indirect calorimeter to assess energy needs in adults and children. Int J Sport Nutr Exerc Metab. 2007;17(5):491-500.

12. Fares S, Miller MD, Masters S, Crotty M. Measuring energy expenditure in community-dwelling older adults: Are portable methods valid and acceptable? J Am Diet Assoc. 2008;108(3):544-548.

13. Holdy KE. Monitoring energy metabolism with indirect calorimetry: Instruments, interpretation, and clinical application. Nutr Clin Pract. 2004;19(5):447-454.

14. Compher C, Frankenfield D, Keim N, Roth-Yousey L; Evidence Analysis Working Group. Best practice methods to apply to measurement of resting metabolic rate in adults: A systematic review. J Am Diet Assoc. 2006;106(6):881-903.

15. Isbell TR, Klesges RC, Meyers AW, Klesges LM. Measurement reliability and reactivity using repeated measurements of resting energy expenditure with a face mask, mouthpiece, and ventilated canopy. JPEN J Parenter Enteral Nutr. 1991;15(2):165-168.

16. Horner NK, Lampe JW, Patterson RE, et al. Indirect calorimetry protocol development for measuring resting metabolic rate as a component of total energy expenditure in free-living postmenopausal women. J Nutr. 2001;131(8):2215-2218.

17. Audrain JE, Klesges RC, DePue K, Klesges LM. The individual and combined effects of cigarette smoking and food on resting energy expenditure. Int J Obes. 1991;15(12):813-821.

18. Kinabo JL, Durnin JV. Thermic effect of food in man: Effect of meal composition, and energy content. Br J Nutr. 1990;64(1):37-44.

19. Reed GW, Hill JO. Measuring the thermic effect of food. Am J Clin Nutr. 1996;63(2):164-169.

20. Haugen HA, Melanson EL, Tran ZV, Kearney JT, Hill JO. Variability of measured resting metabolic rate. Am J Clin Nutr. 2003;78(6):1141-1145.

21. Bracco D, Ferrarra JM, Arnaud MJ, Jéquier E, Schutz Y. Effects of caffeine on energy metabolism, heart rate, and methylxanthine metabolism in lean and obese women. Am J Physiol. 1995;269(4 Pt 1):E671-678.

22. Arciero PJ, Bougopoulos CL, Nindi BC, Benowitz NL. Influence of age on the thermic response to caffeine in women. Metabolism. 2000;49(1):101-107.

23. Arciero PJ, Gardner AW, Calles-Escandon J, Benowitz NL, Poehlman ET. Effects of caffeine ingestion on NE kinetics, fat oxidation, and energy expenditure in younger and older men. Am J Physiol. 1995;268(6 Pt 1):E1192-1198.

24. Burleson MA Jr, O’Bryant HS, Stone MH, Collins MA, Triplett-McBride T. Effect of weight training exercise and treadmill exercise on post-exercise oxygen consumption. Med Sci Sports Exerc. 1998;30(4):518-522.

25. Plankey MW, Stevens J, Palesch Y, Basile JN, Griffin PR. Stability of basal metabolic rate over selected days of the menstrual cycle. Obes Res. 1995;3(3):301-302.

26. Frankenfield DC, Muth ER, Rowe WA. The Harris-Benedict studies of human basal metabolism: History and limitations. J Am Diet Assoc. 1998;98(4):439-445.

27. Feurer ID, Crosby LO, Mullen JL. Measured and predicted resting energy expenditure in clinically stable patients. Clin Nutr. 1984;3:27-34.

28. Frankenfield DC, Rowe WA, Smith JS, Cooney RNN. Validation of several established equations for resting metabolic rate in obese and nonobese people. J Am Diet Assoc. 2003;103(9):1152-1159.

Learning Objectives
After completing this continuing education exercise, the student will be able to:

1. Define “indirect calorimetry” and list areas of research and clinical nutrition therapy in which it is useful.

2. List and discuss four primary components of daily energy expenditure.

3. Trace the evolution of technology and list various methods for gas analysis and collection.

4. Discuss some of the issues and concerns involved in the proper running of indirect calorimeters.

5. Explain why anxiety and other conditions may affect measurements and what precautions and restrictions on behavior and environment should be imposed.

6. List and discuss seven factors affecting resting energy expenditure (REE).

7. Explain why test duration is important and cite the optimal measurement plan.

8. Compare four common REE equations with results obtained by indirect calorimetry.

Examination
1. Indirect calorimetry provides an assessment of resting metabolic rate through the measurement of inspired _____ and expired _____ concentrations.
a. oxygen, carbon dioxide
b. oxygen, nitrogen
c. carbon dioxide, nitrogen
d. carbon dioxide, oxygen

2. A respiratory quotient (RQ) of 0.7 suggests the oxidation of which substrate?
a. Carbohydrate
b. Fat
c. Protein
d. Alcohol

3. If RQ values during indirect calorimetry are outside of the normal physiological range (ie, less than 0.67 or greater than 1.3), it is best to repeat the resting metabolic rate test.
a. True
b. False

4. Basal (resting) energy expenditure typically comprises ____ of total daily energy expenditure.
a. 50% to 60%
b. 80% to 90%
c. 60% to 70%
d. 30% to 40%

5. To improve the accuracy of indirect calorimetry measurements, testing is best done in the early morning hours.
a. True
b. False

6. All of the following factors may influence the accuracy of indirect calorimetry measurements except:
a. menstrual cycle phase.
b. stress/anxiety.
c. food/energy intake.
d. aging.

7. The greatest determinant of resting energy expenditure is an individual’s:
a. fat-free mass.
b. bone mass.
c. brain mass.
d. fat mass.

8. Although it is commonly used in clinical practice, the Harris-Benedict equation has been show to ______ an individual’s REE.
a. overestimate
b. underestimate

9. A decrease in energy expenditure per kilogram body weight often accompanies:
a. aging.
b. caffeine ingestion.
c. increased physical activity.
d. stress/anxiety.

10. When testing young women, it is best to measure resting energy expenditure during the first 10 days of the menstrual cycle, during the _____ phase.
a. luteal
b. follicular
c. thyroid
d. fasting

Extended Bibliography
American Dietetic Association Evidence Analysis. Energy expenditure: Measurement versus estimation. Available at: http://www.adaevidencelibrary.com/topic.cfm?cat=1151

What's new on the Evidence Analysis Library. ADA Times. 2008:16.

Harris JA, Benedict FG. A Biometric Study of Basal Metabolism in Man. Washington, DC: Carnegie Institute of Washington.

da Rocha EE, Alves VG, da Fonseca RB. Indirect calorimetry: Methodology, instruments and clinical application. Curr Opin Clin Nutr Metab Care. 2006;9(3):247-256.

Wooley JA. Indirect calorimetry: Applications in practice. Respir Care Clin N Am. 2006;12(4):619-33.

Weir JB. A new method for calculating metabolic rate with special reference to protein metabolism. J Physiol. 1949;109(1-2):1-9.

Koot P, Deurenberg P. Comparison of changes in energy expenditure and body temperatures after caffeine consumption. Ann Nutr Metab. 1995;39(3):135-42.

Klesges RC, DePue K, Audrain J, Klesges LM, Meyers AW. Metabolic effects of nicotine gum and cigarette smoking: Potential implications for postcessation weight gain? J Consult Clin Psychol. 1991;59(5):749-752.

Perkins KA, Epstein LH, Stiller RL, Marks BL, Jacob RG. Acute effects of nicotine on resting metabolic rate in cigarette smokers. Am J Clin Nutr. 1989;50(3):545-550.

Poehlman ET. A review: Exercise and its influence on resting energy metabolism in man. Med Sci Sports Exerc .1989;21(5):515-525.

Molé PA. Impact of energy intake and exercise on resting metabolic rate. Sports Med. 1990;10(2):72-87.

Short KR, Sedlock DA. Excess postexercise oxygen consumption and recovery rate in trained and untrained subjects. J Appl Physiol. 1997;83(1):153-159.

Willms WL, Plowman SA. Separate and sequential effects of exercise and meal ingestion on energy expenditure. Ann Nutr Metab. 1991;35(6):347-356.

Freedman-Akabas S, Colt E, Kissileff HR, Pi-Sunyer FX. Lack of sustained increase in VO2 following exercise in fit and unfit subjects. Am J Clin Nutr. 1985;41(3):545-9.

Bahr R. Excess postexercise oxygen consumption—magnitude, mechanisms and practical implications. Acta Physiol Scand Suppl. 1992;605:1-70.

Solomon SJ, Kurzer MS, Calloway DH. Menstrual cycle and basal metabolic rate in women. Am J Clin Nutr. 1982;36(4):611-616.

McClave SA, Snider HL. Dissecting the energy needs of the body. Curr Opin Clin Nutr Metab Care. 2001;4(2):143-147.

LaForgia J, van der Ploeg GE, Withers RT, et al. Impact of indexing resting metabolic rate against fat-free mass determined by different body composition models. Eur J Clin Nutr. 2004;58(8):1132-1141.

Bosy-Westphal A, Reinecke U, Schlorke T, et al. Effect of organ and tissue masses on resting energy expenditure in underweight, normal weight and obese adults. Int J Obes Relat Metab Disord. 2004;28(1):72-79.

Mifflin MD, St Jeor ST, Hill LA, et al. A new predictive equation for resting energy expenditure in healthy individuals. Am J Clin Nutr. 1990;51(2):241-247.

Owen OE, Holup JL, D'Alessio DA, et al. A reappraisal of the caloric requirements of men. Am J Clin Nutr. 1987;46(6):875-885.

Owen OE, Kavle E, Owen RS, et al. A reappraisal of caloric requirements in healthy women. Am J Clin Nutr. 1986;44(1):1-19.

Thompson J, Manore MM. Predicted and measured resting metabolic rate of male and female endurance athletes. J Am Diet Assoc. 1996;96(1):30-34.

Cunningham JJ. A reanalysis of the factors influencing basal metabolic rate in normal adults. Am J Clin Nutr. 1980;33(11):2372-2374.

De Lorenzo A, Bertini I, Candeloro N, et al. A new predictive equation to calculate resting metabolic rate in athletes. J Sports Med Phys Fitness. 1999;39(3):213-219.

Table 1. Energy and Respiratory Equivalent of the Three Main Fuels

Oxidized fuel	O2 (l/g) consumed during oxidation	CO2 (l/g) produced during oxidation	RQ	Heat produced/gram oxidized (kcal)	Heat produced/liter O2 consumed (kcal)	ATP equivalent of O2 (mol/mol)
Glucose Lipid Protein	0.746 2.019 0.966	0.746 1.425 0.774	1 0.7 0.8	3.74 9.46 4.32	5.01 4.69 4.48	3 2.85 2.25