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Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL 23610
3 To whom correspondence should be addressed. E-mail: hillr{at}mail.vetmed.ufl.edu.
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ABSTRACT |
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 TOP ABSTRACT LITERATURE CITED |
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KEY WORDS: • energy • dogs • cats • diet history • calorimetry
Dogs and cats require energy to maintain metabolic processes at rest. In addition, they require energy to assimilate food, to maintain body temperature, for activity, reproduction, and growth, and when stressed by disease. Determining how much to feed a dog or cat to provide the metabolizable energy (ME)4 necessary to maintain these processes is the first step in any nutritional recommendation. Subsequently, the nutrient density relative to ME within food must be adjusted to ensure that enough essential nutrients are consumed to maintain normal health while maintaining normal body weight (BW) and body condition score (BCS).
Energy and nutrient recommendations for maintenance of adult dogs and cats by the National Research Council (NRC) (1) and the Association of American Feed Control Officials (2) are based on the requirements of average unstressed healthy adult laboratory dogs and cats, of normal BW and BCS, undertaking modest amounts of exercise in a thermoneutral environment to which they have been adapted. Requirements for growth, pregnancy, and lactation are based on healthy laboratory animals under similar conditions. Most clinical patients do not conform to these norms. Many patients are not healthy, are of different breeds, are over- or underweight, undertake more or less activity than laboratory dogs or cats, and may be exposed to high or low ambient temperatures. For individual patients, therefore, energy expenditure (EE) may be below or above that suggested by the NRC, and the nutrient density of foods may need to be adjusted up or down to ensure adequate but not excess intake of essential nutrients.
Unfortunately, determining the energy needs of any individual animal is not straightforward because there is no readily available point-of-care method of measuring EE in individual animals. Most clinicians, therefore, estimate the energy needs of an individual patient either by a factorial calculation of EE or from a detailed diet history. The purpose of this paper is to discuss the relative merits of factorial calculation, diet histories, and other methods for estimating EE in individual patients. It is hoped that this will spur further research to fill in the manifest gaps in our knowledge concerning the EE of individual patients.
Calculating energy expenditure using a factorial method
Currently, feeding guidelines provided by clinicians and manufacturers mostly rely on calculations. Feeding guides on dog food labels, for example, often follow the NRC recommendation that an average intact active adult pet dog should be fed 
130 kcal ME/kg BW0.75 daily (1). For cats, the 1986 NRC recommendation was that cats required 80 kcal/kg BW daily when active and 70 kcal/kg daily when inactive (3), but this recommendation resulted in too large an estimate for the EE of large cats. The latest NRC recommendations are that normal adult lean cats require 100 kcal ME/kg BW0.67 daily, and obese cats require 130 kcal ME/kg BW0.4 daily (1).
As discussed previously, most patients do not conform to the norm of an average laboratory animal on which these estimates are based, so most clinicians use a factorial approach to estimate EE that takes into account the breed, sex, age, BW, BCS, and physiological state of each patient. A typical recommendation is to calculate the "resting energy expenditure" (REE) in kilocalories ME from body weight in kilograms (kg BW) using an equation such as REE = 70 x kg BW0.75 or REE = 70 + 30 x kg BW. This REE is then multiplied by factors that allow for breed, physiological state, activity, or stress of the patient to obtain the daily energy requirement (4). Thus, for example, multiplying REE by a factor of 2 for a young active dog would give a daily maintenance ME requirement in kilocalories of 2 x 70 x kg BW0.75, that is, 140 kcal ME/kg BW0.75 daily. The problem with this factorial calculation is that a clinician must make decisions concerning which exponent, which BW, and which factor to use, and none of these decisions is straightforward.
The value of the exponent to use with BW when calculating EE has been the subject of much discussion. It is of comparatively little importance, however, because small changes in the value from that recommended by the NRC result in only small changes in the final estimate of EE unless the patient is very large or very small (1). Whether to use current or ideal BW is of much greater importance because many clinical patients are below or above ideal BW, and the effect on the final estimate of EE can be substantial. Each point on a 9-point BCS scale represents a change in body weight of 10–15%, so ideal BW may be as much as 50% above or below current BW, and consequently, the estimate of EE obtained from BW may be affected by a similar amount (5). Unfortunately, there is little consensus and almost no objective data as to whether current or ideal BW provides a better estimate of EE in obese patients (6). Diez et al. reported that obese Beagles with a BCS of 4.3 on a 5-point scale maintained BW when consuming 160 kcal ME/kg ideal BW0.75, and this had to be reduced to 97 kcal ME/kg ideal BW0.75 daily for neutered male patients and 71 kcal ME/kg ideal BW0.75 daily for intact female patients to reach their ideal BW (7). Most reports, however, have been concerned primarily with reducing food intake to induce weight loss and have not reported EE in obese animals before weight loss. The method of calculating ideal BW and then EE has also been inconsistent (6,8,9). Nevertheless, it seems more likely that ideal BW would provide a better estimate of EE than current BW because the increase in fat mass is much greater than the increase in muscle mass in obese patients, and fat mass contributes comparatively little to EE compared with lean body mass (10). In contrast, in patients that are underweight and have not eaten for some time, feeding too much food may induce potentially lethal refeeding or hyperalimentation syndrome (11). In these severely malnourished patients, it would seem wise to use current BW to calculate estimated EE and to use ideal BW to estimate EE only after electrolyte deficiencies have been corrected. A further complication is provided by obese cats that have stopped eating and have developed hepatic lipidosis. These cats often have a high BCS using traditional scoring systems but little muscle mass. The relation among EE, BCS, and ideal BW in these patients needs investigation.
The factor by which REE or basal metabolic rate (BMR) must be multiplied to allow for a patient's particular breed, life stage, or physiological state potentially has the greatest effect on the final estimate of EE, but the appropriate factor to use in many situations remains unclear. Thus, the EE of Newfoundland dogs is known to be much lower than that of Great Danes (1), but it is unclear whether the EE of other large breeds such as the St. Bernard would be similar to the EE of a Newfoundland or of a Great Dane. Dietary thermogenesis appears to add 10% to EE in dogs fed enterally (1), but we have no information about dietary thermogenesis after parenteral feeding in dogs and none concerning dietary thermogenesis in cats fed either enterally or parenterally. Taking account of dietary thermogenesis, the mean resting fed metabolic rate (RFMR) for an average dog would be expected to be 10% higher than the mean for BMR; that is, if the mean for BMR is 76 kcal ME/kg BW0.75 daily, the mean RFMR would be 84 kcal ME/kg BW0.75 daily (1). This RFMR represents the energy that would be required by an enterally fed normal adult dog in a cage undertaking no activity. It might be expected that the energy required for assimilation of nutrients would be less for nutrients provided parenterally than for nutrients provided enterally, but, in humans, dietary thermogenesis appears to be the same whether patients are fed enterally or parenterally (12,13). Currently, therefore, no change is probably necessary when estimating EE in dogs fed parenterally compared with when dogs are fed enterally. It is also likely that dietary thermogenesis adds a similar 10% to the BMR of cats, but the BMR of cats is unknown, so the exact value for dietary thermogenesis in cats is currently a moot point.
Dogs and cats require energy to maintain their body temperature in cold and warm ambient temperatures (approximately a 2-fold increase at 0°C in short-haired breeds) (1). Energy is not expended to maintain body temperature by most hospitalized dogs, however, because the room temperature in most hospitals is within the thermoneutral zone of dogs. Some patients may be exposed to low ambient temperatures when they are exercised, but the extra EE associated with activity probably provides enough heat to maintain body temperature in the cold. Cats appear to have a high thermoneutral zone and may require increased energy to maintain body temperature even at room temperature, but most measurements of EE in cats have been performed with cats at room temperature, so no allowance for the effect of ambient temperature is probably necessary in hospitalized cats (1).
Energy requirements also change with disease or stress, but how much EE changes with disease or stress in dogs and cats remains uncertain. In human patients, EE increases up to 2-fold, depending on the severity of the disease process, but recent studies suggest that feeding more conservatively may be beneficial. Thus, in humans, total EE increases dramatically after thermal injury so that patients burned over 40% of their body surface area may require 2 times predicted basal EE (14). Nevertheless, feeding burn patients >1.2 times REE resulted in increased fat mass without any increase in lean body mass (14). Similarly, metabolism increases with sepsis, but experimental studies in several species suggest that moderate underfeeding (providing approximately two-thirds of expected energy requirements) improves survival (15).
Changes in EE have been measured using indirect calorimetry in a few dogs with naturally occurring disease, but most of these measurements have been performed after only short (15 min) periods of adaptation to the procedure. Indirect calorimetry requires collection of expired gases, usually with a mask or from within a chamber in which the subject is confined. Procedures such as these can be stressful to dogs and cats and are likely to increase EE unless animals are adapted to the procedure for several weeks. The stress of the procedure may mask disease-induced changes in EE or suggest disease-induced changes in EE that are not present. Thus, the EE of dogs with osteosarcoma was 20% higher before surgery and 12% higher after surgery compared with EE in control dogs, but control dogs were adapted to the measurement procedure over several weeks, whereas the dogs with osteosarcoma appear not to have been adapted in the same way (16). Similarly, EE measured with only 15 min adaptation was reported to be almost 20% lower in dogs with lymphoma than in control dogs (16,17). Energy expenditure measured in unadapted dogs with lymphoma and nonhematological tumors was unchanged after treatment (17,18) and did not change from before to immediately after surgery for orthopedic disease (19). In unadapted dogs, EE was not different between control and critically ill dogs (20). Daily EE in unadapted dogs was also lower in hypothyroid dogs before treatment than after treatment (mean ± 2 standard deviations were 78 ± 35 vs. 99 ± 42 kcal/kg BW0.75), but half the patients were obese before treatment, and the authors did not account for any change in body weight with treatment (21). In each study, EE in unadapted unfed control dogs was higher than has been previously reported in adapted dogs (1). Others have found that mean EE increased by 35% 2 h after the onset of sepsis and 1 d after severe burn injury induced experimentally in dogs (22,23). Review of all these flawed data suggests that changes in EE in dogs and cats with disease may be more modest than would be suggested by studies of human patients and that estimates of EE in dogs and cats either should not be increased or increased by only a small amount to allow for illness. Moderate underfeeding may also improve the prognosis of animals with sepsis.
More is known about the energy required by dogs and cats for exercise, but there remain many unanswered questions. For animals running on a treadmill, the increase in EE for activity is proportional to the distance traveled irrespective of speed: dogs weighing >10 kg BW require1 kcal ME/kg BW, and smaller dogs and cats require 1.6–1.9 kcal ME/kg BW, for each kilometer traveled (1). This is in addition to the energy required for standing, which is 50% more than the energy required by animals lying down. Additional energy is needed when dogs or cats run over rough terrain, through snow, climb or run up and down a hill and run into a headwind or when dogs carry or pull a load (1).
Thus, EE is much less for dogs that run short distances such as greyhounds than for dogs that run long distances such as hunting dogs and sled dogs. A 30-kg BW greyhound with a BMR of 1000 kcal ME and a maintenance energy requirement of 2000 kcal ME requires only 15 kcal to run 500 m. Even allowing for the additional energy required for acceleration at the start of a race, this 30-kg BW greyhound would use <40 kcal for a 500-m race (1). Racing greyhounds in training require on average only 140 kcal ME/kg BW0.75 daily (2 times BMR), whereas sled dogs require as much as 1050 kcal ME/kg BW0.75 (>10 times BMR) (1). Also, EE is higher for terriers, which stand for long periods of the day even when confined in the home, than in large dogs that lie down for most of each day in the home. If the amount of activity is known, therefore, the energy required for activity might be estimated, but deciding how much activity is actually being undertaken by an individual dog or cat is very difficult.
In humans, some indication of the EE for activity for an individual may be obtained by keeping an "activity record" of the type and duration of each activity during each day. Tables that list the EE associated with each type of activity in humans can then be used to estimate the total EE for activity for that individual during each day (24). There are no such tables of activity EE for dogs and cats, nor is there information concerning the EE for running over rough ground, pulling loads, swimming, grooming, climbing, or jumping. There is also no information concerning the energy requirements of dogs undertaking many activities, such as agility trials or "big air" jumping, or concerning differences in the energy needed for horizontal movement in different breeds. Finally, there are no standardized methods of classifying the duration or severity of activity. Activity records are, therefore, currently of no value for estimating EE in dogs and cats.
There is considerable information concerning changes of EE for growth, lactation, and gestation (1), but application to clinical patients is not always routine. The normal estimates for ME requirements for growing puppies (2–3 times what would be expected for maintenance of an adult dog of the same BW), for example, make allowance for increased activity as well as for growth. When a puppy is hospitalized, however, EE decreases because activity decreases, but how much should ME intake be reduced to allow for this change without affecting growth? Similarly, ME requirements appear to decrease with neutering and age, but some of the change in EE may be caused by changes in lean body mass and activity. How much, therefore, should the estimate of total EE be adjusted in sedentary hospitalized patients that are either above or below ideal body weight at different stages of their life?
A further fundamental problem with factorial calculations is that they do not account for individual variation. Recommendations for EE in all these examples have been based on the mean EE of groups of animals, whereas EE in dogs and cats, even for specific groups of animals under closely defined physiological conditions, have shown wide variability about the mean. For example, the mean measured daily BMR of dogs is 76 kcal ME/kg BW0.75, but BMR in individual dogs has varied from 30% below to 50% above this mean (1). Similarly, the variance of EE of Alaskan sled dogs running the same distance at the same rate under the same conditions suggests a range from 20% above to 20% below the mean (1). Among cats, measurements of ME requirements have also shown great individual variation, and the NRC guidelines suggest that individual cats may require 50% more or less than a mean estimate (1). At present, therefore, factorial calculations are only an educated guess of the actual energy requirement for an individual animal and may be incorrect by a substantial margin. This could lead to embarrassment if, for example, a veterinarian overestimates the EE for an obese patient and the patient proceeds to gain rather than lose weight following that recommendation. Nevertheless, factorial calculation still provides a readily available rapid method of estimating the EE of hospitalized patients. Also, comparison of actual ME intake with expected ME intake based on NRC recommendations may be of value to ascertain whether essential nutrient intake is likely to be adequate when a commercial diet is fed, as commercial diets are designed to contain enough essential nutrients when the expected amount of ME is consumed.
Diet histories and weighed records
Obtaining a detailed and accurate diet history remains the best method of estimating the ME requirements of an individual pet that is maintaining BW and BCS in the home environment because it takes individual variation into account and allows for differences in activity and environment. Nevertheless, diet histories of human food consumption are notoriously inaccurate (25), and clinical experience suggests that owners are not much more accurate when reporting food consumption by their pets. For human patients, a "weighed record" of food consumed correlated better with EE than did a diet history, but both weighed record and diet history correlated poorly (r2 < 0.35) with EE when EE was measured using the double-labeled water (DLW) method (26,27). Activity records have also proved inaccurate in humans (28). The repeatability of a detailed questionnaire of canine dietary intake was high but lower for home-cooked foods than for commercial foods (29). Energy intake obtained from this detailed dietary questionnaire also correlated moderately well with energy intake obtained from a weighed record of dog food consumption (r2 = 0.67) (29). Nevertheless, detailed diet histories are difficult to obtain, time consuming, and, therefore, potentially prohibitively expensive. Most owners feed treats and supplements, which makes the diet complex to assess. Most owners do not initially confess or remember all that they have fed, and most do not accurately measure how much is given. The size of cup used to measure food is often not standard, and it may be necessary to ask an owner to make a weighed record of all food consumed over a week to obtain an accurate measure of food intake.
Determining the ME density of a weighed amount of food can also be difficult. The ME density of most human foods can be obtained from commercial databases or the internet, but the type of human food must be carefully described because ME density may change with the method of food preparation and manufacturer. Estimating the ME density of commercial pet foods can be even more difficult. Some manufacturers report average analyses and ME densities of their foods, but others report only guaranteed analyses. It is possible to estimate the average analysis from the guaranteed analysis but only by making several assumptions. First, comparison of the guaranteed analysis with the average analysis where both have been reported suggests that commercial foods contain 1% more crude fat and crude protein than the reported guaranteed minimum for these nutrients and 1% less moisture and crude fiber than the guaranteed maximum for moisture and fiber. It is possible, therefore, to estimate the average analysis of these nutrients by making a small 1% correction from the reported minimum and maximum for each of these nutrients. In practice, however, this slight correction has only a small effect on ME density, whereas the ash content of the diet has a much greater effect on ME density because ash content varies greatly among diets. The ash content is often not included in the guaranteed analysis and must be guessed before the carbohydrate content of the diet can be estimated by difference. Once the average analysis has been estimated, however, the ME density of the diet can be estimated using Atwater or modified Atwater factors. The 1985 NRC nutrient guidelines recommended using modified Atwater factors (30) to determine the ME density of pet foods, but doing so underestimates the ME density of low-fiber, high-fat digestible foods and overestimates the ME of high-fiber foods. The latest NRC guidelines attempt to correct for such differences in digestibility among diets by adjusting gross energy for energy digestibility estimated from the fiber content of the food and should provide better estimates of the ME density of commercial foods (1).
Thus, obtaining an estimate of ME intake from a diet history or weighed record represents the best method of estimating the EE of a free-living individual animal undertaking consistent amounts of activity because it takes individual variation into account, but it has the potential for error and can be prohibitively expensive to perform. A diet history or weighed record is of less help in hospitalized patients, however, because the ME intake when an animal is free-living must be decreased to allow for the change of activity when an animal is hospitalized. Such a change immediately adds error because it relies on a factorial reduction in EE based on an estimate of the change in activity.
Other methods for measuring energy expenditure in dogs and cats
If EE could be measured directly, then food intake could be adjusted for each individual. Various methods have been used to measure EE of humans, but few have been evaluated for use in dogs and cats (25). Indirect calorimetry remains the gold-standard method for measuring EE. It relies on the principle that the energy released from nutrients oxidized in the body can be deduced from the rate of oxygen consumption and carbon dioxide production in the body. Energy utilization can be deduced if oxygen and carbon dioxide concentrations in expired breath and the rate of flow of expired breath are measured. Indirect calorimetry has been used to measure the EE of dogs and cats at rest and running on treadmills (1), but the equipment is expensive, requires some training to use reliably, and is not available in most hospitals. Indirect calorimetry is also of limited use in clinical patients because dogs and cats take several weeks to adapt to the procedures used for collecting expired gas. Small single-use indirect calorimeters and portable devices have been used to measure EE in human patients at rest and during exercise, respectively (31,32), but neither has been adapted for use in dogs and cats.
The DLW method deduces EE from the rate of production of carbon dioxide within the body. The rate of carbon dioxide production can be deduced from the differential rate of washout of stable isotopes of hydrogen and oxygen (2H and 18O) after water enriched with both of these isotopes has been introduced into the patient (33). This method has been validated in dogs (34) and has been used to measure energy consumption in free-living dogs (35,36). It is an excellent method for measuring average energy consumption over 1 to 2 wk because the rate of excretion of the isotopes of hydrogen and oxygen is relatively slow. The DLW method has not been widely used, however, in dogs and cats because DLW has been prohibitively expensive, and isotope measurement requires a mass spectrometer. Activity in dogs and cats is also episodic and varies in quality and quantity from minute to minute, so the DLW method cannot be used to assess the EE of dogs undertaking short-duration activity or for clinical patients whose energy needs vary from day to day.
It is also possible to estimate the rate of carbon dioxide production (and thus EE) from the rate of washout of the stable or radioactive isotopes of carbon (13C and 14C, respectively) after bicarbonate enriched with one of these isotopes has been introduced into a patient. Stable isotope measurement also requires a mass spectrometer, but labeled bicarbonate is less expensive than DLW, and the turnover of labeled carbon within the body is rapid, which allows carbon dioxide production and therefore EE to be measured over minutes to hours. This labeled bicarbonate method has been used to measure energy utilization at rest and during short bouts of exercise in a few species (37,38). There is only one such report in dogs, which describes the use of a constant infusion of bicarbonate labeled with 13C to measure energy consumption in resting dogs (39). Continuous infusion of labeled bicarbonate is impractical, however, in free-living dogs. The labeled bicarbonate and DLW methods also do not measure oxygen utilization and, therefore, depend on an assumption concerning the average respiratory quotient over the period of measurement to determine oxygen utilization. As a result, these methods have a greater potential for error than methods that do measure oxygen consumption (10).
Measurement of heart rate with heart rate monitors has been used to estimate EE indirectly in humans, but there are no reports of this approach in dogs and cats. In humans, heart rate is related to oxygen consumption and EE during exercise but not at low heart rates (25). Heart rate also varies with age, physical fitness, physiological state, and with excitement, so the relation between heart rate and oxygen consumption needs to be established for each individual (25). Simple heart rate monitors may also not be able to measure the very rapid heart rate that can be observed in dogs and cats during vigorous exercise.
In our laboratory we have used Holter monitors (Dual Channel Electrocardiorecorder, Del Mar Avionics) to record the electrocardiogram of racing greyhounds before and after a race but not to measure EE. Some dogs did not run well because their running action was affected by the weight of the tape recorder, but a typical trace (Fig. 1) illustrates other problems associated with measuring heart rate in exercising dogs. Heart rate was low when dogs were resting and did increase when EE would have increased as dogs walked to the track, but heart rate increased with excitement at the track even when dogs were standing still. Heart rate then increased to well over 200 beats per minute while dogs were waiting in the starting box for the arrival of the lure. Motion artifact also prevented accurate measurement of heart rate during the race, and heart rate remained very high for many minutes during recovery after the race, when energy expenditure would have been low again. It seems unlikely, therefore, that heart rate monitors will provide a good estimate of EE in dogs.
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In summary, assessing energy consumption in free-living patients is very difficult. Currently, a factorial calculation based on population means is the most common method used to estimate EE in clinical patients but requires many assumptions and educated guesses and does not allow for individual variation. A complete diet history and a weighed record of food consumed provides the best method of assessing the energy required by free-living individuals but is time consuming and expensive. There is a great need for a readily available point of care test that will measure EE in clinical patients, but none is currently available.
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FOOTNOTES |
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2 Author disclosure: Expense for the author to travel to the symposium and honoraria were paid by the WALTHAM Centre for Pet Nutrition. The author is The WALTHAM Associate Professor of Small Animal Internal Medicine and Nutrition at the University of Florida.
4 Abbreviations used: BCS, body condition score; BMR, basal metabolic rate; BW, body weight; DLW, double-labeled water; EE, energy expenditure; ME, metabolizable energy; NRC, National Research Council; REE, resting energy expenditure; RFMR, resting fed metabolic rate.
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