Modern Nutrition in Health and Disease 10th Edition

2006 Lippincott Williams & Wilkins

49 Body Composition and Anthropometry

1

Steven B. Heymsfield Richard N. Baumgartner A persons body composition reflects his or her total lifetime nutrient and energy balance. Maintaining optimum health requires the maintenance of adequate tissue levels of essential nutrients and a source of energy. More than 40 syndromes develop if tissue levels of these are either too low or too high (1). Anthropometry is the science of estimating or predicting body composition based on measurements of weight, stature, body circumferences, and subcutaneous fat thicknesses. This chapter describes methods for predicting protein and energy stores from anthropometry because most patients seen for clinical evaluation have a disorder of protein -energy balance (2,3). This is prefaced by a discussion of the principles underlying energy and protein balance and body composition m odels.

ASSESSMENT COMPONENTS Steady-State Relations

The concept of steady -state relations between energy exchange and protein stores is important because disruptions result in disordered body composition and associated pathologic features. The difference between energy intake and expenditure affects three main body composition components, the small storage carbohydrate glycogen pool, the larger structural and functional protein pool, and the variable lipid or fat storage pool ( Fig. 49.1). Taken together with associated water and minerals, the collective energy compartment is reflected by and changes parallel with body mass. Body weight is therefore a fundamental measurement in nutritional assessment because it is an indirect marker of protein mass and energy stores. The consequences of weight change depend on initial body composition. Weight loss in a frail elderly patient with sarcopenia (low muscle mass), whether voluntary or involuntary, conveys very different risks than weight loss in a middle-aged overweight patient with adequate muscle mass. Weight loss involves the depletion of body nutrient stores. The excessive depletion of protein stor es, whether from wasting or cachexia, results in the loss of specific cellular and tissue functions, with consequences ranging from loss of cell-mediated immunity to cognitive impairment. Conversely, weight loss in an overweight or obese person with adequa te protein stores mainly consists of loss in fat mass, which improves certain cellular and tissue functions, for example by reducing levels of oxidative stress and improving insulin sensitivity and glucose and lipid metabolism. A major portion of tissue function can be attributed to proteins that are activated by energy derived from

metabolism of organic fuels ( 4). As an organic compound, protein is also a metabolic fuel, and, under conditions of weight stability, oxidation of amino acids provides about 15% of daily energy requirements ( 5). The energyproducing reactions take this general form:

Urea is not metabolized further and is excreted unchanged in urine. During periods of nutritional deprivation, approximately half the total body protein mass can P.752 be used as metabolic fuel ( 6). A greater loss of protein is incompatible with survival. Therefore, when food intake is less than nutrient losses, amino acids from proteins are oxidized to provide energy, various tissue functions are altered, and, ultimately, protracted negative protein balance results in a rapid rate of lean tissue depletion and death. The extent to which this occurs depends on the availability of other nonprotein energy stores.

Figure 49.1. Interrelations between energy intake, output, and stores. (Data from Heymsfield SB, Baumgartner RN, Pan S-F. Nutritional assessment of malnutrition by anthropometric methods. In: Shils ME, Olson JA, Shike M, eds. Modern Nutrition in Health and Disease. 9 t h ed. Baltimore: Williams & Wilkins, 1999:903 21; and Heymsfield SB, Hoffman DJ, Testolin C et al. Evaluation of human adiposity. In: Bjrntorp ed. International Textbook of Obesity. Chichester, UK: John Wiley & Sons, 2001:85 97.) The main sources of nonprotein energy are glycogen and fat or triglyceride. Glycogen is stored primarily in liver and skeletal muscle ( 7). Glycogen stores are small (<400 g), and carbohydrate oxidation on a usual diet in the United States accounts for about 50% of daily energy production (5). Fat is found almost entirely within adipocytes or fat cells (8). A small amount of lipid is also present within muscle

and liver cells (9). Fat stores vary widely in humans, with fatty acid oxidation representing about 35% of energy production in the average US diet ( 5). Both glycogen and fat are oxidized in reactions similar to that for protein (Equation 1), except urea is produced only with amino acid oxidation. The sum of protein, glycogen, and fat constitutes total body energy content. These fuels account for more than 90% of the nonaqueous portion of body weight ( 10). Generalizations can be made on how body weight, protein, glycogen, fat, and energy stores relate to each other. Glycogen and protein are both solubilized by water and electrolytes. About 2 to 4 g water will bind to 1 g of either glycogen or protein (11). Changes in glycogen or protein balance are thus associated with greater changes in body weight than can be attributed to loss of the actual chemical component. For example, oxidation and loss of 100 g glycogen would result in approximately a 0.5 -kg reduction in body weight. The main remaining chemical components exclusive of fat are minerals, found primarily in the skeleton ( 8,10). The total fat-free portion of body weight thus consists of protein, glycogen, water, and minerals ( Fig. 49.2). In healthy adults, the steady -state fractional contribution of three of these components to total fat-free mass (FFM) is reasonably constant: protein = 0.195, water = 0.725, and mineral = 0.08, respectively. Glycogen levels vary throughout the day and represent a fraction of FFM in the range of 0.01 to 0.02. With long -term weight loss, the change in FFM is approximately the same as the relative reduction in protein (1). Acute changes in body weight and FFM may also reflect alterations in glyc ogen and fluid balance.

Figure 49.2. The first four of the five levels of human body composition. Components related to fatness are identified by bold enclosure. ECS and ECF are extracellular and intracellular solids, respectively. (From Bistrian BR, Blackburn GL, Vitale J et al. JAMA 1976 ;235:156770, with permission.) Fat maintains a relatively constant, although more complex relation to fat-free components. Figure 49.3 shows a plot of total body fat(TBF)/height 2 versus body weight/ height 2 in 414 women. Fat was measured in the women using a four component model (8). The ratio body weight/ height 2 , referred to as body mass index ( BMI, kg/m 2 ), is P.753 discussed later in more detail. Two important points are related to this figure. First, the intercept for zero TBF is a

BMI of approximately 13, which represents a woman without any fat and minimal protein stores, a condition incompatible with survival. Second, the slope of the regression line (i.e., the change in fat adjusted for stature/the change in body weight adjusted for stature) of approximately 0.74 indicates that body weight added above a BMI of about 13 is predicted to be about three fourths fat and one fourth FFM. The composition of excess weight, however, may differ between men and women and vary with race, age, and disease (12). Figure 49.4 shows how the relationship between BMI and percentage of body fat changes with age in healthy women and men. With increasing age, any measured BMI corresponds to a higher level of body fat, owing to the slow, age -related loss of muscle mass, or sarcopenia (13,14).

Figure 49.3. Relationship between total body fat (measured by four component model [8]) adjusted for stature and body mass index (BMI) in 414 healthy women (R 2 = 0.91, p < .001). In summary, body weight is a general, indirect marker of protein mass and energy stores. A loss or gain in body weight is usually assumed to reflect proportional changes in protein and energy stores. How this relationship varies with gender, race, and age, and particularly in relation to disease, is important for correct interpretation of anthropometric measurements used to estimate or predict fat and protein stores, as described in later sections of this chapter.

Figure 49.4. Total body fat, expressed as a percentage of body weight, versus body mass index in females ( upper panel) and males (lower panel). The regression lines were developed based on the formula of Gallagher and associates [#6] (39).

Figure 49.5. Model depicting changes in metabolic balance and body composition in protein -energy malnutrition and obesity. Point A is the range of body composition and tissue function found in health. Weight is stable, and balances of energy, nitrogen (N), and water are zero. Disease causes negative metabolic balance, weight loss, and changes in body composition and tissue function. Point B u is the minimal range of body composition and tissue function that is compatible with survival. The course of a patient moving between points A and B u may be interrupted by a

complication related to malnutrition, and this is indicated by point C u . Positive balance leads to obesity, and a similar set of end points, B o and C o , is designated.

Balance
Body composition is in a dynamic state over time. Both total body protein mass and energy content decline between meals as a result of obligatory amino acid oxidation and metabolism of other fuels ( 7,15). The result is negative protein and energy balance. With food intake, balance becomes positive, and total body protein and energy content increase. Over a typical day, net protein and energy balance are zero, and body weight remains cons tant. These relations are depicted in Figure 49.5, in which point A represents an optimal state in which long -term balance is zero and health risks are minimal (1). If the individual at point A develops an acute or chronic illness, then food intake may be inadequate to replace nutrient losses, so net energy and nitrogen balance become negative and body weight is lost. If the condition persists and balance remains negative, the subject ultimately approaches the poi nt at which survival is no longer possible (B u ). Loss of functional proteins and other essential nutrients results in the clinical complications described at the beginning of this chapter and shown in Figure 49.5 as C u . Clinically significant abnormalities in P.754 physiologic function and loss of total body protein are seen in most hospitalized patients who lose more than 20% of their preillness body weight (16).

Conversely, overeating relative to nutrient utilization results in positive balance and, if sustained, causes weight gain (B o ). The maximum survivable body weight is approximately 500 kg or a body BMI of approximately 150. As with undernutrition, obesity is associated with complications (C o ). The discovery that adipose tissue does not function merely as a storage organ for excess energy, but also acts as an endocrine organ that participates with the brain and other peripheral tissues to regulate metabolism as well as immune function, has revol utionized the understanding of the mechanisms that underlie the health complications of obesity. Figure 49.5 embodies the main aims of nutritiona l assessment: to define the patients status relative to points A, B, and C, and four specific questions:

What is the patients body weight and body composition status relative to arbitrarily defined normal or healthy values for gender, age, and race? If the patient is determined to be either undernourished or overnourished, what are the mechanisms leading to either negative or positive nutrient balance? Is the patient at risk of developing health complications as a result of their altered nutritional status? With nutritional treatment is balance altered, and, over time, is the patients weight and body composition moving toward the healthy range?

Function

An important assumption of nutritional assessment is that body composition is an indirect measure of cellular function. Body composition estimates are usually highly correlated with specific functional tests. For example, anthropometric midarm muscle area is strongly correlated with forearm grip strength (17). However, body composition should not be assumed equivalent to tissue function; the two are different types of biologic measurements that serve different purposes but can, under certain c onditions, be used in exchange for one another. An example in which mass and function can dissociate is the case of a patient with cardiomyopathy. Massive enlargement of the heart muscle is possible, yet the capacity of the myocardium to generate force and eject blood into the systemic circulation is severely impaired. The distinction between body composition estimates and cellular function indices should be kept in mind when evaluating the results of a patients anthropometric and biochemical evaluations ( 16).

ANTHROPOMETRY
Anthropometry was originally developed in the late nineteenth century by anthropologists to quantify variation in human form across age, gender, and racial groups. Its use for assessing nutritional status was first realized in the late nineteenth century by Richer, who used skinfold thickness as an index of fatness ( 18). The modern era of nutritional anthropometry began with the studies of Matiegka during World War I ( 19). Matiegkas interest in the physical efficiency of soldiers led him to develop methods of anthropometrically subdividing the human body into muscle, fat, and bone. Anthropometric techniques are now widely used in many areas of human biologic r esearch (20,21,22).

The purpose of nutritional anthropometry is to quantify the amount and distribution of the major nutritionally relevant components of body weight. A full ap preciation of anthropometric measurements requires an understanding of human body composition and its organizational levels. Human body composition can be studied at five levels: I, atomic; II, molecular; III, cellular; IV, tissue -system; and V, whole-body (8). The first four levels and their major components are shown in Figure 49.2. Accurate methods have been developed for estimating components at each of these levels. It is important to understand the merits and limitations of these methods because anthropometric techniques are usually d eveloped using one or more of these as the reference standard.

BODY COMPOSITION MODELS Atomic

The first level of body composition consists of 11 elements that comprise more than 99.5% of body weight. The primary elements are oxygen, hydrogen, carbon, nitrogen, and calcium. Triglycerides stored in adipose tissue are composed of carbon, hydrogen, and oxygen in proportions of approximately 76.7, 12.0, and 11.3%, respectively; protein is 16.1% nitrogen; and bone mineral is about 39.8% calcium (23,24,25,26,27,28). These stable elemental proportions allow the calculation of TBF, protein, and mineral masses from measurements of elemental masses. Whole -body measurements at this level are generally made by in vivo neutron activation analysis methods ( 24,25,26,27). Anthropometric methods, however, are available for estimating total body nitrogen, calcium, and potassium at the atomic level based on prediction equations developed by

statistical regression of anthropometric measurements on these elemental measurements ( 25).

Molecular
The second level of body composition consists of the major molecular components that comprise body weight, particularly water, protein, glycogen, mineral (osseous and nonosseous), and lipid that can be quantified in vivo ( 23). Total body lipid includes triglycerides, sphyngomyelin, phospholipids, steroids, fatty acids, and terpenes. The term total body fat, however, generally refers to triglycerides, which are the primary storage lipids in humans and P.755 comprise nearly 90% of the total lipid component. TBF can be estimated using a two -component model in which the molecular level is simplified to body weight = TBF + FFM. Several two-component methods are used to estimate either TBF or FFM, including underwater weighing, total body potassium, and total body water ( TBW) (23). Each method relies on one or more assumptions that relate measurable body composition quantities to the unknown component of interest. As an example, FFM can be estimated from TBW, as measured by isotope dilution analysis, by assuming that FFM has an average hydration of 73% (i.e., TBW/FFM = 0.73 or FFM = TBW/0.73). TBF can then be calculated as the difference between body weight and estimated FFM. The assumption that FFM is 73% water has been shown to be valid across a wide range of species, including humans (28,29). Another commonly applied two -component method is underwater weighing, which is based on the relatively stable

densities of fat (0.9007 g/cm 3 ) and FFM (1.100 g/cm 3 ). In this method, body density (D b ) is measured by immersing the subject in a specially designed water tank and using Archimedes principle of buoyancy or water displacement. Newer methods using air displacement have also been developed (30). TBF is then estimated from D b and body weight using the following equation: Which, by algebraic rearrangement, gives the following: However, the assumption of a constant FFM density of 1.100 g/cm 3 causes some model error as FFM density actually varies, although within a relatively narrow range. To avoid this model error, three -, four-, and/or five-component models were developed for measuring TBF with improved accuracy (31). Dual-energy x-ray absorptiometry (DXA) has emerged as an increasingly popular method of estimating three molecular level components: TBF, total body bone mineral (TBBM) and lean soft tissue mass (LST), where FFM = TBBM + LST. This method is based on the differential attenuation of photons at low and high energy levels within a scanning x -ray beam. Elements of low atomic weight, such as hyd rogen, minimally attenuate photons, whereas elements such as calcium are highly attenuating. The ratio of high to low energy attenuation is specific to each element and therefore to each molecular component. As the x -ray beam scans a persons body on a pix el-by-pixel basis, the quantities of mineral, fat, and lean soft tissue are calculated for each pixel based on the measured attenuation ratios and calibration equations. The values for all pixels scanned are then summed to estimate these molecular level co mponents

for the whole body. Various studies have established that DXA estimates are highly precise and generally accurate. The main limitation is that the accuracy of the DXA method is influenced by the thickness of the energy absorbing tissues in the pat h of the x-ray beam. Thus, accuracy decreases when scanning either very thin subjects, such as infants, or thick subjects, such as obese adults ( 32,33). The molecular level of body composition is important in nutritional assessment because fat and FFM are the major components in which en ergy stores are distributed. Fat has an energy density of 9.4 kcal/g, and all but 1 to 2 kg is metabolically available during periods of protracted negative energy balance. Protein and glycogen have respective energy densities of 5.65 and 4.1 kcal/g. Assum ing that the proportions of protein and glycogen are relatively normal in FFM, the metabolically available energy from FFM is 1.02 kcal/g (34,35). Accordingly

Half of the energy contained within FFM can usually be used as fuel during long-term semistarvation (35). The estimation of TBF and FFM thus allows the calculation of total body energy content and thereby changes in energy balance over time. FFM is generally accepted as an index of protein stores, and changes over time are assumed to represent alterations in protein balance. Resting oxygen consumption, carbon dioxide production, and heat production (i.e., energy expenditure) are all highly correl ated with FFM, and FFM accounts for approximately 50 to 80% of the individual variation in energy expenditure ( 36). Thus, resting

metabolic rate (RMR, kcal/day) is commonly estimated from FFM using prediction equations such as ( 37): where FFM is in kilograms. Such equations have always been recognized as being somewhat imprecise, specifically at the extremes of body weight. Recently, Mller and colleagues (38) published new equations for children and adolescents and adults that may provide somewhat better accuracy across a range of BMIs for use in white populations (see Appendix Table A -10-f). Anthropometric methods are available for estimating TBW, FFM, and TBF at the molecular level (20, 21, 23, 25, 39,40,41).

Cellular
The cellular level of body composition consists of three main components: cells, extracellular fluid, and extracellular solids (8). Measurement techniques are available for quantifying extracellular fluid and solids, although total cell weight or the weight of specific cell groups is difficult to quantify in vivo. A widely used model of body composition at this level was suggested by Moore and his colleagues (40). Total cell mass was considered to be composed of two components: fat (a molecular level component) and fat -free, or body cell mass (BCM), the component responsible for most of the bodys metabolic processes. P.756 Moore and associates proposed that total body potassium, or exchangeable potassium, which is approximately equivalent in amount, could be used to estimate BCM because the potassium concentration of intracellular fluid is relatively constant at 150 mmol/L, and the ratio of

intracellular fluid to s olids is approximately 4:1 (i.e., intracellular fluid = BCM 0.80). BCM could then be calculated using these relations combined with an estimate of either total body or exchangeable potassium (i.e., BCM = [total body potassium/150] [1/0.80] or total body potassium 0.0083). The equation for body weight according to Moore and his colleagues was thus equal to fat + BCM + extracellular fluids and solids. Cells are the main functional components, and quan tification of BCM enables investigators to explore important physiologic and functional relations. At present, several anthropometric equations can be used to predict BCM at the cellular level (40).

Tissue-System
The tissue-system level of body composition consists of the major tissues and organs. Body weight at this level is equal to the sum of adipose tissue, skeletal muscle, bone, and visceral organ masses. Human adipose tissue is often assumed to be on average of 80% lipid, 14% water, 5% protein, and less than 1% mineral, and a density of 0.92 g/cm 3 at body temperature (42). In truth, there is actually large variation in adipose tissue composition. Level of adiposity, age, gender, and heredity all play important r oles in determining adipose tissue composition, notably fat content. Adipose tissue is distributed into subcutaneous, visceral, and interstitial anatomic compartments. Subcutaneous adipose tissue is generally defined as that between the fascia of skin and the muscles. Visceral adipose tissue is defined as that surrounding the organs, or viscera, in the thorax, abdomen, and pelvis. Interstitial adipose tissue is

interspersed between cells within a tissue, particularly skeletal muscle. The proportions of tota l adipose tissue in these compartments are not constant and are under hormonal and genetic control, with metabolic properties of adipose tissue varying among different anatomic locations (43). Men, elderly persons, and obese subjects tend to have a higher percentage of total adipose tissue in the visceral compartment than women, young, and lean subjects, respectively (43,44). Obese, elderly, and physically inactive subjects tend to have a higher proportion of interstitial adipose tissue (45). This component is also increased in many muscle diseases, such as Duchene musc ular dystrophy. Weight gain or loss is associated with different relative rates of adipose tissue change in these compartments as well as from different subcutaneous sites (46). This differential loss of adipose tissue is important when interpreting anthropometric measurements. A strong positive correlation exists between the amount of visceral adipose tissue and the health risks of obesity. Skeletal muscle is the largest component within the adipose tissue-free body mass, accounting for approximately half of adipose tissue-free body mass in healthy adults ( 8,9). Skeletal muscle consists of muscle tissue, nerves, and tendons. Approximately 20% of adipose tissue -free skeletal muscle is protein, and muscle is the largest tissue reservoir of amino acids (6). Depletion of up to 75% of skeletal muscle mass is possible during pro longed semistarvation (6). Skeletal muscle mass decreases with age after about 45 years, with greater losses in men than women ( 47). This age-related loss leads to a state of deficient muscle mass, or sarcopenia, in many elders in which protein stores are insufficient for an adequate response to the physiologic

stresses posed by acute or chronic illnesses. Sarcopenia is accordingly associated with age -related impairment of thermogenesis and immunocompetency, functional limitation and disability, and increased risk of falls a nd bone fractures, and sarcopenic elders are particularly vulnerable to weight loss (48). In about 10% of elders, a condition known as sarcopenic obesity may develop in which muscle mass is reduced in the presence of excess adipose tissue mass ( 49). Careful evaluation of body composition is needed for these persons because the excess mass of adipose tissue may obscure their low muscle mass and vulnerability to weight loss. The response of visceral organs to semistarvation is variable. Organs decrease in weight at different rates during uncomplicated semistarvation. For example, liver mass decreases rapidly in rodents with underfeeding, whereas heart weight decreases at about the same rate as body weight (46). The pattern of visceral organ changes in protein-energy malnutrition associated with physiologic stress may differ from that of uncomplicated underfeeding. An example is the severe weight loss that often accompanies metastatic malignant disease. Cancer cachexia in both animals and humans is accompanied by preservation of some visceral organs despite loss of body weight and atrophy of skeletal muscles ( 50). The preservation of visceral organs with physiologic stress may represent an adaptive response to injury or infection that is the anatomic counterpart to increased synthesis of serum acute -phase reactants. Magnetic resonance imaging and computed tomography are used by investigators to quantify total body and regional adipose tissue and skeletal muscle ( 8,23). Imaging and

ultrasonic techniques can also be used to estimate visceral organ and skeletal weights. Skeletal muscle and adipose tissue are important components in nutritional assessment because they are readily estimated by anthropometric techniques. At present, many anthropometric equations can be used to predict total and visceral adipose tissues, skeletal muscle, and bone mass at the tissue -system level (8,51,52).

Whole-Body
The whole-body level of body composition includes the main anthropometric dimensions of weight, stature, P.757 circumferences, breadths, and skinfold thicknesses. Other whole-body measures include body weight, volume, density, and electrical impedance.

Features of the Model

The five-level model has several important features. First, the model is consistent as a whole and each component is distinct (8). Connections between components are important in relation to anthropometric methods, however. An example is a group of related components at atomic to tissue -system levels, calcium, bone mineral, extracellular solids, skeleton, and bone breadths. Each of these components is distinct, and yet all five are linked because they are different constituents or dimensions of the human ske leton (8). Second, steady-state relations exist between many components at the same or different levels ( 8). Steadystate as defined here means a stable relation between components over a specified time interval, usually months or years. Some steady -state relations were described

earlier, such as the hydration of FFM = 0.73 and intracellular potassium concentration = 150 mmol/L. These quantitative associations are important in developing body composition models that relate a known component to an unknown component of interest. The steady -state relations are particularly important in the field of anthropometry because all anthropometric measurements are at the whole body level, and yet they are used primarily to infer information about the first four body composition levels. It is important to understand how steady -state relations are altered by gender, age, race, and disease and thus change the quantitative associations established between anthropometric dimensions and other body components. The following is a summary of anthropometric method s in the context of the five -level model.

Measurements
The anthropometric measurements generally used for nutritional assessment include body weight, stature, skinfolds, circumferences, and bone breadths. These whole body measurements can be used in indice s or prediction equations to estimate the values of components at the other four levels (Table 49.1). The following discussion groups the various anthropometric measurements and techniques into three categories: (a) body weight and stature; (b) estimates of fatness and energy stores; and (c) lean tissue indices, protein mass, and functional components. TABLE 49.1. SOME CHARACTERISTIC COMPONENTS AT LEVELS I TO IV AND RELATED ANTHROPOMETRIC MEASURES AT LEVEL V

CHARACTERISTIC COMPONENTS

ANTHROPOMETRIC MEASURES AT LEVEL V BRE ADT

LE LE VE L I T B C VE L II F at

LE VE L III F at c el ls LEV EL IV Adi po se tis su e B W X STA TUR E CIRCU MFERE NCES X X SKIN FOLD S

HS SKE LET AL

T B O

T B W

B C M + E C F

AT FW

T B C a, T

M o

E C S

Bo ne, sk ele ton

B P

T B N, T B K

Pr o, M s

B C M

Mu scl e + vis cer a

T B N a, T B Cl

M S

E C F

Blo od + IS F

ATFW, adipose tissue -free body weight; BCM, body cell mass; BW, body weight; TBW, total body water; ECF, extracellular fluid; ECS, extracellular solids; ISF, interstitial fluid; Pro, protein; Mo, bone mineral; MS, soft tissue mineral; TBC, TBCa, TBCl, TBK, TBN, TBNa, TBO, TBP: total body carbon, calcium, chloride, potassium, nitrogen, sodium, oxygen, and phosphorus, respectively; TBW, total body weight; levels I to V: atomic, molecular, tissue-system, and whole -body levels of body composition, respectively.

Body Weight and Stature

Body weight is the sum of all components at each level of body composition. As described earlier, body weight is a rough measure of total body energy stores, and changes in weight parallel energy and protein balance. A significant correlation exists (r = 0 .6, p < 0.05) between loss of body weight and change in total body protein in seriously ill adults (14). Body weight usually varies less than 0.1 kg/day in healthy adults. A loss in weight of more than 0.5 kg/day either indicates negative energy or water balance or a combination of the two. Clinically significant weight loss is considered a relative decrease in weight of more than 10% over a ti me interval of less than 6 months ( 1). The severity of weight loss in an individual person is determined by two factors: the rate of weight chang e over time and the total reduction in weight. The rate of weight loss in total starvation is approximately 0.4 kg/day, and survival is sustained to about 70% of desirable (i.e., ideal) body weight (1). Semistarvation, the more typical cause of negative energy balance in patients, results in a more gradual loss in weight compared with that in total starvation. In patients with chronic disease, the weight change may occur over years or decades. The minimal survivable body weight in humans is between 48 and 55% of desirable body weight or a BMI of approximately 13 (i.e., point B u in Fig. 49.5). Body weight at this point consists of less than 5% metabolically available fat ( 1). Exhaustion of the remaining usable fat mass results in rapid depletion of lean tissue and death.

The absolute body weight and rate of change in weight have prognostic value, and two aspects are recognized. The first is that an absolute body weight of less than 55 to P.758 60% of desirable places the subject at or near the survival limits of starvation (1). Further negative balance could not be tolerated for long. The second aspect is that a significant reduction in body weight from preillness weight (between 10 and 20%) over a time interval of less than about 6 months places the patient at risk of developing functional impairment of multiple org an systems and an adverse clinical outcome. Studley was among the first to associate weight loss with disease outcome (53). In 1936, this pionee ring investigator made the classic observation that marked weight loss before surgical procedures for peptic ulcer resulted in a higher postoperative mortality rate relative to that in weight -stable patients. Modern workers have identified weight loss as a major determinant of prognosis in many disease states and conditions, such as survival time in patients with carcinoma of the colon and chronic obstructive lung disease ( 54,55). Seltzer and his colleagues found a 19 -fold increase in mortality in adult patients undergoing elective surgery who lost more than 10 lb body weight preoperatively compared with patients with no or small weight loss ( 56). Hirsch and associates obse rved a 21% preoperative weight loss in patients who died postoperatively compared with a 12% preoperative weight loss in survivors ( 57). An important study by Windsor and Hill refined Studleys classic observation by demonstrating that the postoperative patients with weight loss who are at the highest risk of

complications are those who also have clinically obvious impairment in organ function ( 58). Postoperative patients with clinically apparent organ impairment in this study also had significant abnormalities of a variety of measured physiologic functions and a reduced weight of total body protein. Summarizing this and other studies from his laboratory, Hill concluded that a weight loss of less than 10% of preillness body weight is usually not associated with functional abnormalities; a weight loss of between 10 and 20% of preillness body weight is accompanied by functional abnormalities in some patients; and a weight loss of more than 20% of preillness body weight is associated with protein-energy malnutrition and multiple functional abnormalities in almost all patients ( 14). Weight loss is thus an important indirect index of multiple physiologic functions the underlying severity of disease and a guide to a patients prognosis. Body weight is measured longitudinally to establish the effectiveness of nutritional therapy. A change in weight reflects energy, protein, and water balance.

Measurement.
In the hospital, body weight shoul d be measured within 0.1 kg on a calibrated physicians scale. Special scales should be used in bedridden or wheelchair -bound patients. Edema, if present, should be recorded with the weight. The general procedure is to obtain a morning weight following evacuation of the bladder. The weight of the hospital gown can be subtracted from the total weight if the desired goal is nude weight. When comparing the patients weight with standard values, the patients attire is usually presented in a footnote on the ta ble. Serial weights should be measured

on the same or a carefully calibrated scale. Intake and output records may be useful in interpreting the significance of changes in weight. Height is usually measured by a sliding bar attached to the physicians scale , although more accurate techniques are used for research purposes. Height can be estimated in bedridden patients using knee height or arm span prediction equations (Table 49.2) (59,60,61,62). Knee height is measured in the sitting position with an anthropometric caliper. The bottom of the patients foot is placed flat on the floor and forms a right angle wi th the knee. The heel is raised, and the caliper blade is placed under the heel. The calipers movable blade is then lowered to the top of the thigh at a minimum of 2 inches posterior to the kneecap. Methods for recumbent measurement of knee height are als o available. Arm span is defined as the distance between the tips of the longest finger of each hand with subjects standing erect against the wall and both arms fully stretched horizontally ( 60,62).

Interpretation.
Interpretation of body weight as an index of available energy supply must be used with caution in four conditions:

Edema and ascites cause a relative increase in extracellular fluid and may mask loss in chemical or cellular components. Massive tumor growth or organomegaly can mask loss in fat or lean tissues such as skeletal muscle. Lean tissue and cellular atrophy are partially masked by residual fat and connective tissue in obese patients undergoing rapid or severe weight loss. Patients may still be overweight and yet suffer severe protein -

energy malnutrition and also be at increased risk of adverse health outcomes secondary to semistarvation.

Large changes in energy intake cause corresponding changes in glycogen mass and bound water over several days. Similarly, large changes in sodium intake are associated with brief period s of fluid readjustment and body weight change.

For these reasons, and also to provide a more complete characterization of body composition, anthropometric methods are used to assess body weight further. These methods are described under two general headin gs as they relate to nutritional assessment: measures of fat stores and measures of lean tissues. Reference tables provide a standard weight for height, and in some cases an adjustment is made for frame size (see Appendix Tables A 12 and 14 to 16).

Fat
Although fat refers specifically to a chemical component at the molecular level of body composition, this section as a P.759 whole relates to the following five -level sequence: atomic, carbon; molecular, fat; cellular, fat cells; tissue -system, adipose tissue; and whole-body, anthropometric dimensions (e.g., skinfolds and circumferences) (see Table 49.1). Anthropometric measurements are well suited for estimating fatness because the subcutaneous adipose is readily accessible and measurable. Although more accurate and reproducible methods of estimating fatness exist, anthropometric methods are the simplest, safest, most practical, and least costly of the available techniques.

TABLE 49.2. RECOMMENDED EQUATIONS FOR PREDICTING STATURE IN ADULTS AND CHILDREN a

AGE GROUP White men GROUP 1860 1767 6080 1767 1767 EQUATION Stature = 1.88(knee height) + 71.85 Stature = 2.3(knee height) + 51.1 Stature = 2.08(knee height) + 59.01 Stature = 2.30(knee height) - 0.63(age) + 54.9 Stature = 0.762(arm span) + 40.7 REFERENCE 49 50 51 50 50

Black men

1860 6080

Stature = 1.79(knee height) + 73.42 Stature = 1.37(knee height) + 95.79

49 51

White

1860

Stature =

49

women

2271 2271 6080 2271

1.87(knee height) - 0.06(age)+ 70.25 Stature = 1.84(knee height) + 70.2 Stature = 1.91(knee height) - 0.098(age)+ 71.3 Stature = 1.91(knee height) - 0.17(age)+ 75.0 Stature = 0.693(arm span) + 50.3

50 50 50 50

Black women

1860 6080

Stature = 1.86(knee height) - 0.06(age)+ 68.1 Stature = 1.96(knee height) + 58.72

49 51

White boys

618

Stature = 2.22(knee height) + 40.54

49

Black

618

Stature =

49

boys

2.18(knee height) + 39.6

Chinese boys

416

Stature = 0.92(arm span) + 10.84

52

White girls

618

Stature = 2.15(knee height) + 43.21

49

Black girls

618

Stature = 2.02(knee height) + 46.59

49

Chinese girls

416

Stature = 0.93(arm length) + 10.34

52

Arm span, knee height, and stature in cm; age in

years.

The amount of fat in healthy subjects varies greatly, with relatively small amounts in some highly trained athletes and relatively large amounts during the later stages of pregnancy. During protracted undernutrition, all but a small amount of TBF can be used as metabolic fuel (1). Two factors determine the adequacy of fat: the amount of total body triglyceride present and energy balance. Very littl e fat is sufficient if the person is healthy and in zero energy

balance. In contrast, a small amount of fat in the presence of marked negative energy balance implies a limited survival time. The usual practice is to compare fat values from an individual patient with reference standards and also to follow trends over time. During nutritional therapy, the measurement of fat provides an indirect guide to energy balance.

Measurement and Interpretation.

Four methods of assessing fatness are available: (a) the single skinfold method, (b) the limb fat area method, (c) TBF (or adipose tissue) calculated from multiple anthropometric measurements, and (d) TBF from the difference between body weight and FFM predicted from anthropometry and bioelectric impedance measurements. The fourth method is indirect, depending on the primary estimation of TBW or FFM, as discussed further later in the section on bioimpedance analysis (BIA) . Skinfold thicknesses are additionally used to describe the anatomical variation in subcutaneous fat thickness, or fat pattern, and waist circumference is used as an index of the amount of visceral adipose tissue. The measurements common to these techniques are now briefly reviewed, and the interested reader should consult additional references for added details (20,21,22). Skinfolds represent a double layer of subcutaneous tissue, including a small and relatively constant amount of skin and variable amounts of a dipose tissue, and they are measured with specially design calipers. The caliper should be a rugged and light instrument, and jaw pressure should be maintained at 10 g/mm 2 throughout the measurement range. The contact surface area of the jaws can vary

between 30 and 100 mm 2 , and the jaws on some calipers remain parallel as they are opened wider. The essential technique is to pinch and elevate a skinfold at specific anatomic sites using the thumb and fingers and to measure the thickness of the fold with the calipers. These measurements are correlated with, but are not directly representative of, the actual thickness of subcutaneous adipose tissue. It is important to make repeated measurements because errors will occur. Standardized measuring techniques and me thods for optimizing precision should be carefully followed ( 20,21,22). Skinfold measurements are not accurate in massively obese patients, and they are not useful for predicti ng amounts of intraabdominal adipose tissues. Commonly measured skinfold thicknesses include: biceps, triceps, subscapular, suprailiac, thigh, and calf ( 1). The absolute skinfold thickness can be used directly for comparison with reference tables and for longitudinal P.760 follow-up (see Appendix Tables A -16 and A-17 and subdivisions). The limitation of evaluating one skinfold thickness is that a single measurement is a relatively poor predictor of the absolute amount and rate of change in TBF because (a) large interindividu al differences exist in fat distribution, (b) as TBF changes, each skinfold site responds differently relative to changes in TBF, and (c) the relationship between skinfold thickness and TBF is complex (e.g., an exponential relationship exists between subcutaneous skinfold thickness and TBF and between subcutaneous fat and visceral fat) ( 51,63). Other factors that limit a single skinfold thickness as a measure of fatness

include changes in the composition of adipose tissue with age and nutritional status; variation in skinfold distribution and compressibility with age; and the inclusion of a small amount of nonadipose tissues (e.g., skin) in the measurement (1,21,51). The final consideration is that the day-to-day variability in measuring the same skinfold is large, even when the rigorous procedures are followed. Measuring skinfold thickness should therefore be considered a qualitative measure of the amount and rate of change in TBF. The advantages are ease and rapidity of measurement, especially in bedridden patients. Standardized methods have been developed for measuring body circumferences, or girths, on the limbs and trunk that can be also used to estimate body fa tness and grade body fat distribution. Body circumferences are useful in that, unlike skinfold thicknesses, they can always be measured, even in extremely obese subjects. They reflect internal as well as subcutaneous adipose tissue, but they are also influenced by variation in muscle and bone. As a result, the interpretation of circumference measurements, and especially circumference ratios, is often not straightforward. As for all anthropometric variables, body circumferences should be measured with close attention to standardized procedures (19). Flexible, inelastic cloth, and steel tapes are recommended. The tape measure should be durable, should resist stretching, and have an accuracy of 0.1 cm. The most useful circumferences for grading or predicting body fat and for describing adipose tissue distribution are upper arm, chest, waist or abdomen, hip or buttocks, proximal or midthigh, and calf ( 20). Waist or abdomen circumferences are usually very highly correlated with total fat mass and percentage of body fat in men (r > 0.85); in

women, hip or thigh circumferences may have slightly higher correlations. Correlations of upper arm, thigh, and calf circumferences with measures of body fat are somewhat lower, and these circumferences tend to be more strongly influenced by variation in appe ndicular skeletal muscle. Waist circumference and ratios of waist to hip or thigh circumference are widely used to grade or estimate visceral adiposity, which is recognized as the main aspect of adipose tissue distribution that is associated with increased risk of chronic disease (64). Waist circumference is now used in conjunction with BMI to classify persons into risk levels for chronic disease. Risks are increased for BMIs greater than 25 kg/m 2 when waist circumference is greater than 108 cm in men and 88 cm in women ( 65). Zhu and colleagues (66) also developed cutpoints for grading chronic disease risk specifically from waist circumference. Their analysis indicated that a waist circumference greater than 100 cm in men and 93 cm in women was associated with a disease risk equivalent to a BMI greater than 30 kg/m 2 , indicating the need for clinical weight loss. Combining a limb skinfold thickness with a corresponding circumference allows calculation of limb fat areas using the following general equation:

where C is a limb circumference measurement (i.e., upper arm, midthigh, calf), and SF is a skinfold measurement taken at the same level as the circumference measurem ent following standard methods. Most of the problems related to a single skinfold measurement also occur with the limb fat area. The advantage generally ascribed to area calculations is that the result includes the contribution of limb

circumference; two limbs with equal skinfolds but unequal circumferences will have different amounts of fat. Many prediction equations are available for calculating TBF from measured skinfold thicknesses, circumferences, body weight, and stature. All the present methods in us e are descriptive in that measured anthropometric dimensions are converted to TBF or other components using statistically derived equations in the absence of an underlying theory or mechanism. In contrast, some body composition methods are based on theor etic or mechanistic models (e.g., BCM is calculated from exchangeable potassium using a model that assumes a constant intracellular potassium concentration). All descriptive methods, including anthropometry, share in common the following: development in a well-defined subject group, use of a criterion method for estimating TBF, and a prediction model formulated using regression analysis. Some methods, for convenience and speed, are based only on gender, body weight, stature, and circumferences (67,68). As all prediction formulas are population specific, they should be cross -validated in new subject groups before application. Ideally, the fat -prediction formula would be used in a group similar to the population on whom it was developed. A good example and most widely applied TBF prediction formula was developed by Durnin and Womersley using underwater weighing as the criterion for fat estimation ( 69) (Table 49.3). The sample consisted of 209 white men and 272 women who were less than 68 years of age and on average were normal or slightly overweight. Once TBF is known, it can be subtracted from body weight to provide a value for FFM.

TABLE 49.3. CALCULATION OF FAT AND FAT -FREE BODY MASS ACCORDING TO THE METHOD OF DURNIN AND WOMERSLEY

1. Determine the patients age and weight (kg)

2. Measure the following skinfol ds in mm: biceps, triceps, subscapular, suprailiac

3. Compute the sum () of these skinfolds

4. Compute the logarithm of

5. Apply one of the following age - and sex-specific equations to compute body density (D, g/mL) AGE RANGE (y) 1719 MEN D = 1.1620 0.0630 (log) WOMEN D = 1.1549 0.0678 (log)

2029

D = 1.1631 0.0632 (log)

D = 1.1599 0.0717 (log)

3039

D = 1.1422 0.0544 (log)

D = 1.1423 0.0632 (log)

4049

D = 1.1620

D = 1.1333 -

0.0700 (log)

0.0612 (log)

50+

D = 1.1715 0.0779 (log)

D = 1.1339 0.0645 (log)

6. Fat mass (kg) is then calculated as: FM = Body weight (kg) [4.95/D - 4.5]

7. Fat-free mass (FFM) (kg) = Weight (kg) - Fat mass (kg)

P.761

A literature search will turn up many fat -prediction formulas that are applicable in specific populations and that vary in use of measurement type (i.e., circumferences and skinfolds) and anatomic location. Some examples of methods in current use for femal e subjects are presented in Table 49.4. In most of these formulas, the dependent (i.e., predicted) variable is D b . These methods were developed using underwater weighing as a reference for D b estimation and anthropometric dimensions along with other covariates such as age were set in regression models as independent variables. The anthropometric predicted density can be converted to percentage of fat using traditional two component body composition models, as outlined in Table 49.4. The advantages of calculating TBF are that (a) more than one skinfold site is usually included in the calculation and

(b) the result (in kilograms) can be used directly to calculate energy reserves as fat. The latter values can then be integrated with estimates of energy balance calculati ons, thus providing a more physiologic description of the patients nutritional state. A cautionary note is that, as with all prediction equations, results are most accurate on populations on which the equation was derived. The accuracy of the Durnin -Womersley equation and those presented in Table 49.4 is unknown in patients with severe weight loss, and the techniques should not be applied when a gross distortion in body habitus or obvious fluid accumulation is present ( 69). As emphasized by Damon and Goldman, skinfold thicknesses describe, but do not measure, TBF (70). The error of prediction of TBF from skinfolds may be considerable in some persons even when group means are accurate. More accurate methods of measuring fat are therefore usually applied in research studies of body composition. TABLE 49.4. ANTHROPOMETRIC EQUATIONS THAT PREDICT BODY DENSITY IN THE FEMALE POPULATION a

AUTHOR S (DATE; REF.) Katch & McArdl e (1973; EQUATION Density = 1.09246 [0.00049 (scapula n 69

MEAN OR RANG E 25.6 6.4% r 0.8 4 SEE 0.008 6 (3.6 %)

106)

SF)] [0.00075 (iliac SF)] + [0.00710 (ED)] [0.00121 (thigh C)]

Jackson et al. (1980; 107)

Density = 1.1470 [0.0004293 (chest SF + midaxillary SF + triceps SF + subscapular SF + abd SF + suprailiac SF + thigh SF)] + [0.00000065 (7SF) 2 ] [0.00009975 (A) [0.00062141 5 (gluteal C)]

24 9

4 44%

0.8 7

0.007 9 (3.6 %)

Wright

Density =

18

0.7

(4.1

et al. (1980; 108)

[1.051 (biceps C)] [1.522 (forearm C)] - [0.879 (neck C)] + [0.326 (abd 2 C)] + [0.597 (thigh C)] + 0.707

37%

%)

Hodgdo n & Beckett (1984; 67)

Density = (0.35004 [log 1 0 (waist C + hip C neck C)] + (0.22100 [log 1 0 (H)]) + 1.29579

21 4

10 47%

0.8 0

0.008 0 (3.7 %)

Vogel et al. (1988; 109)

% Body fat = [0.173 (hip C)] + (105.328 [log 1 0 (Wt)]) - 0.515 (H)] - [1.574 (forearm C)] -

26 6

5 50%

0.7 7

(3.9 %)

[0.533(neck C)] - [0.200 (wrist C)] 35.6

Tran & Weltma n (1989; 110)

Density = 1.168297 [0.00284 (abd C)] + [0.00001220 98 (abd 2 )] [0.00073312 8 (hip C)] + [0.00051047 7 (H)] [0.00021616 (A)]

40 0

35.9 7.7 %

0.8 9

0.009 5 (4.2 %)

A, age (y); Abd, average waist and abdomen at naval

(cm); C, circumference (cm); ED, elbow diameter (cm); H, height (cm); SF, skinfold (mm); Wt, weight (kg). Correlations are show for test group samples unless otherwise specified. The interested reader should consult original source for information regarding application of specific equation.

It is customary to express TBF estimates as a percentage of body weight. A problem in interpreting this approach is P.762

that, as a person gains or loses weight, both fat and FFM change. Additionally, the relationship between body fat and body weight has a nonzero intercept (see Fig. 49.3). The result is that a curvilinear relationship exists among TBF, expressed as a percentage of body weight, and body weight or BMI (see Fig. 49.6). These complex relationships can result in some confusing situations, such as when a severely obese patient loses a relatively large am ount of weight and yet the percentage of fat change is relatively small. A highly trained athlete and a severely malnourished patient may have an equivalent percentage of body weight as fat. They could also have a similar absolute fat weight. To overcome these difficulties, Van Itallie and colleagues suggested calculating a fat (or FFM)-stature index similar to BMI as follows: fat/height 2 (71). A low or high fat mass index would then represent a reduced or increased actual fat mass relative to stature, respectively. For example, fat mass index in a malnourished patient would be lower than in a highly trained athlete, even though both had an equivalent percentage of body weight as fat. This is because the athlete with a similar percentage of body weight as fat would have a much larger absolute fat mass and also a much larger FFM and greater body weight than the malnourished patient.

Figure 49.6. Percentage of body weight as fat in 413 healthy women versus body mass index (BMI). Fat was measured by four component model ( 8).

Lean Tissues
Lean tissues refer in general to the following sequence of components at the five levels of body composition: atomic: nitrogen, potassium, and calcium; molecular: FFM, water, and protein; cellular: BCM; tissue -system: skeletal muscle, skeleton, and visceral organs; whole -body: anthropometric measurements (e.g., skinfolds/circumferences) (see Table 49.1). These various components are associated with the major portion of whole -body metabolic activity and biologic functions.

Semistarvation.
Semistarvation results in negative balances of energy, protein, water, and minerals, a reduction in FFM and BCM,

and atrophy of tissues and organs ( 1,72). Not all lean components change at the same rate during periods of negative balance. At the molecular level, cellular proteins are depleted rapidly, and connective tissue proteins are lost at a slower rate (1). Similarly, at the cellular level, rapid changes can occur in BCM, whereas extracellular fluid is lost more slowly or may even increase in volume ( 72). Organs and tissues also differ in their rate of weight loss during semistarvation. Liver mass decreases rapidly and brain weight changes very little if at all in uncomplicated semistarvation; liver and other visceral organs may be preserved in chronic catabolic conditions such as metastatic malignant diseases (50). Skeletal muscle is a major reservoir of amino acids for acute -phase protein synthesis and can decrease by up to 75% in weight during protein energy malnutrition (6). The malnourished patient with a reduced body weight therefore has a different composition at each of the five levels compared with his or her normally nourished counterpart. This explains why anthropomet ric equations developed in physiologically normal subjects may not predict a specific component with equal accuracy in an undernourished seriously ill patient. In anthropometrically assessing the severity of malnutrition, an important goal is to define the amount and rate of change in total body or skeletal muscle protein ( 6). The main anthropometric indices used for this assessment are FFM (molecular level) and limb muscle areas (tissue -system level). Because lower limits compatible with survival are known for both types of measurement, the severity of protein-energy malnutrition is usually judged as the patients value relative to the normal range on the one hand and the minimal range on the other ( 1). In terms of

prognostic value, these measurements will provide some index of potential survival time; given the patients anthropometric FFM or muscle index and nitrogen balance, progression toward or away from potentially lethal starvation can be established. During nutritional therapy and follow-up, the anthropometric FFM indices are used as measures of nitrogen balance, and specific details regarding interpretation are presented in the following paragraphs.

Measurement and Interpretation.

Measuring FFM is accomplished by anthropometric methods, such as those described earlier in the section on fat. The same cautions in measurement technique and selection of patients noted in the earlier discussion of fat also apply to FFM. With regard to interpretation, in theory multiplying FFM (in grams) by 0.195 and 1.02 provides the amount of total body protein in grams and metabolizable energy in kilocalories. Of the metabolizable energy in the healthy subject, about half of that in FFM is available during prolonged periods of semistarvation ( 1). When combined with balance data and information on TBF, these bedside calculations often provide an interesting insight into a P.763 patients course. Unfortunately, the information needed for accurate prediction of total body protein cannot be derived from anthropometric FFM because of the changes in body hydration and variability of skinfold measurements described earlier. A large tum or burden or organomegaly of any cause may also add mass (as water, protein, and mineral) to FFM that is metabolically unavailable. In patients without serious derangements in body composition,

FFM can be used to calculate RMR as presented earlier in Equation 5. This FFM-based calculation of RMR is largely independent of sex and age although evidence is accumulating that ethnic RMR differences exist even after controlling for body composition ( 36). Calculating the amount of limb muscle tissue from anthropometric data requires only two measurements: the limb circumference and the corresponding skinfold thickness. The midportion of the upper limb is usually studied, and little additional information is gathered by also measuring thigh and calf muscle areas ( 46). Calf muscle measurement would, of course, be useful in subjects whose upper extremities are burned, amputated, edematous, or immobilized by casts or traction devices. The upper arm muscles tend to atrophy slightly more rapidly during semistarvation than the muscles of the thigh or cal f, but the differences are not large ( 46). Equations for estimating limb muscle area from anthropometry take the following general form: where C is a limb circumference (e.g., upper arm, mid thigh, calf), and SF is a skinfold taken at the same level as the circumference using standardized methods. The primary application of limb muscle measurements is to obtain a measure of the amount and rate o f change in skeletal muscle protein. The following three factors should therefore be considered:

The mass of a skeletal muscle represents a three dimensional measurement (i.e., volume), whereas limb muscle area and circumference are two - and onedimensional indices, respectively ( 1,46). As the muscle

changes volume, the corresponding proportional changes in muscle area and circumference will be smaller than the change in volume. For example, a 50% decrease in muscle volume will correspond to a theoretic decrease in muscle area and circumfe rence of 37 and 21%, respectively. As a rule, the relative change in muscle area will be larger than the change in muscle circumference.

The equations for calculating limb muscle indices are based on simple theoretic assumptions regarding arm geometry (1,46). Actually, the calculated arm muscle area overestimates the amount of skeletal muscle by 15 to 25% in relatively young, nonobese subjects. Half of this overestimate results from the inclusion of bone in the calculated area, and the remainder results from errors in the assumptions and t he inclusion of nonmuscle tissue (e.g., neurovascular bundle) in the result (73). Two methods of correcting this overestimate of muscle area are available. The first is to express results as a percentage of standard, because the standard value will also contain these nonskeletal muscle components. The second approach is to calculate bone -free arm muscle area by subtracting a constant value (10 c m 2 for men; 6.5 cm 2 for women) from the arm muscle area estimate obtained by the general equation. Studies by Forbes and Baumgartner and their colleagues suggested that arm muscle area assumptions are also inaccurate in obese and elderly subjects, respectively ( 74,75). Martin and colleagues developed an an thropometric prediction formula for total body skeletal muscle mass, although the accuracy of this method in monitoring

changes in muscle mass and associated protein content has not been reported ( 52). Further studies are therefore needed to improve our understanding of the relationship between anthropometric muscle estimates at the whole-body level of body composition and actual skeletal muscle mass at the tissue -system level.

Atrophic skeletal muscle differs in chemical composition from normal tissue. Per gram of muscle, the amounts of water, total lipid, and collagen are increased, whereas the noncollagen proteins are reduced. Thus, the concentr ation of functional proteins per unit arm muscle area or circumference is relatively lower in the atrophied muscle. Another chemical consideration is that muscle size can abruptly change by 5 to 10% in response to rapid changes in muscle glycogen as a result of the water-binding properties of glycogen (46).

Thus, both anthropometric FFM and muscle indices are truly indirect markers of the active protein component of body weight. The two lean tissue indices should be considered approximate bedside guides to the amount of total body protein. Despite their approximate nature, anthropometric muscle estimates correlate with more complex methods of estimating skeletal muscle (e.g., total limb muscle area versus total body skeletal muscle volume by magnetic resonance imaging; Fig. 49.7) over the broad biologic range of muscle mass in humans. Small changes in total body protein cannot be detected by anthropometry, and nitrogen balance and other techniques must be used for this assessment.

Bioimpedance Analysis

Nutritional assessment using anthropometry is now increasingly augmented through the additional measurement of BIA. This technique is used to predict body composition based on the electrical conductive properties of the human body. The ability of the body to conduct an electric current is the result of the presence of free ions, or electrolytes, in the body water. The amount of electricity P.764 that can be conducted is determined mainly by the total volume of electrolyte -rich fluid in the body. Measures of bioelectric conductivity are therefore proportional to TBW and to body composition components with high water concentrations such as the FFM and skeletal muscle mass. As a result, these methods predict TBW, FFM, and total body skeletal muscle mass. TBF must be derived as the difference between body weight and predicted FFM (76).

Figure 49.7. Correlation between total limb muscle area

(sum of arm, calf, and thigh muscle areas in cm 2 ) and total body skeletal muscle volume in L by whole -body magnetic resonance imaging in healthy subjects. N = 79, Total muscle area (cm 2 ) = 7.6 Skeletal muscle (L) + 115.4, R 2 = 0.6423, p < 0.001. Many factors other than the amount and electrolyte concentration of body water, however, influence measurements of electrical conductivity. These includ e body temperature, distribution of fluids between intracellular and extracellular spaces, body proportions or geometry, the amounts and structures of different conductive, as well as nonconductive, tissues, and technical issues such as correct calibration and application of the equipment. The net result is that exact functional relationships between measurements of bioelectric conductivity and TBW or other fat-free components cannot be derived from either physiochemical models or experimentally. Thus, re lationships between conductivity measurements and body composition components are established indirectly by statistical calibration against criterion measures (e.g., estimates of TBW from deuterium dilution analysis or FFM from DXA) in a sample of subjects (76).

Measurement and Interpretation.

The most commonly used BIA method injects a highfrequency, low-amplitude alternating electric current (50 kHz at 500 to 800 A) into the body using distally placed electrodes and measures the voltage drop caused by resistance with proximal electrodes. Conventionally, surface gel electrodes are used with standardized placements on the right ankle and hand, although other electrode

arrangements have been described that allow estimation of segmental (e.g., arm or leg) electrical properties ( 76). Stainless steel contact electrodes are also now used in some systems in place of the conventional gel electrodes. The amount of resistance measured (R) is inversely proportional to the volume of electrolytic fluid in the body. It is also dependent on the proportions or geometry of this volume (i.e., ratio of length [L] to cross -sectional area [A], or R L/A). These relationships have led to the use of the simple formula V = L 2 /R as the theoretic basis of most BIA applications, where V is conductive volume (e.g., TBW), L is a measure of body length (usually stature), R is measured resistance, and is an estimate of the specific resistivity of the conductive material ( 76). The validity of this simple formula has certain limitations. The formula is accurate only for a cylindric conductor with uniform cross-sectional area and homogenous composition (e.g., a wire). The human body could be described as a series of roughly cylindric conductors with variable cross sectional area and heterogeneous, highly structured composition. The value of is influenced by all these factors and consequently cannot be deduced directly. As a result, equations for predicting body composition must be developed based on independent measurements of resistance, stature, and other anthropometric variables, and TBW or FFM in a sample of subje cts. Least-squares regression techniques are applied to the data to derive an equation of the basic form: where a is intercept, b is slope, and e is residual error or unexplained variation in V caused by random measurement errors and/or misspecification of the parameters (a and b)

in the equation. It is not possible to interpret the parameter b in this equation as an estimate of in the formula V = L 2 /R, unless the intercept (a) and residual error (e) approach zero. These conditions are rarely, if ever, met for the reasons given earlier. BIA prediction equations usually include additional parameters for age, gender, body circumferences, and skinfold thickness. Thus, this method can be considered a supplement to anthropometry for predicting body compositi on in patients. Some equations for predicting TBW, FFM and total body skeletal muscle mass are given in Table 49.5 (77,78,79). TABLE 49.5. EQUATIONS FOR PREDICTING BODY COMPOSITION FROM BIOELECTRIC IMPEDANCE AND ANTHROPOMETRY

Males 1280 y a TBW = 1.203 + 0.176(Weight) + 0.449(Stature 2 /R) FFM = -10.678 + 0.262(Weight) + 0.652(Stature 2 /R) Females 1280 y a TBW = 3.747 + 0.113(Weight) + 0.45(Stature 2 /R) + 0.015(R) FFM = -9.529 + 0.168(Weight) + 0.696(Stature 2 /R) + 0.016(R) Adults 1886 y b Total skeletal muscle mass = 5.102 + 0.401(Stature 2 /R) + 3.825(gender) -0.071(age)

Weight (kg); Stature (cm); R, resistance (ohms); TBW,

total body water; FFM, fat-free mass. TBF, total body fat = Weight FFM.

a b

Data from reference 77. Data from reference 78.

P.765

Similar to anthropometric prediction methods, BIA equations tend to lose accuracy when applied to subjects who do not resemble those included in the sample from which the equations were developed. Thus, their generalizability may be limited and all equations should be prevalidated in a subsample against an accepted reference method before general extension to an entire study population. In clinical application, the user should be aware that large disturbances in body fluid distribution between intracellular and extracellular compartments, for example edem a or ascites, may affect the accuracy of BIA equations for predicting body composition. Conversely, methods have been developed that take advantage of the sensitivity of BIA to alterations of body water distribution in patients with various disorders (80).

Reference Values
Body Weight

The patients body weight is evaluated using two reference sources. The first reference values are those of the patient, and these include a usual weight by history or previous measured weight. This is important because many obese patients who lose weight during an illness and are thus potentially malnourished will still be overweight by conventional standards. T he second reference source is the healthy population. In this approach, the individual persons actual body weight is compared with that of a gender -, stature-, and age -appropriate reference or desirable body weight (see Appendix Tables A -12, A-14, and A-15 and their subdivisions). The subjects actual body weight is expressed as a percentage of desirable. The normal range for desirable body weight varies among different sources, but it usually is set between 90 and 120%. A body weight below or above these levels is consistent with undernutrition and obesity, respectively. Another method of comparing the patients weight with that of a reference population is to calculate a body weight (BW)-stature (S) index (81). Most weight-stature indices in present use take the form W/S p (69). The term p indicates how stature is to be scaled. The main assumptions of weight-stature indices are that they are independent of height, represent an indirect index of body composition, correlate with health outcomes, and can be generalized across different populations. The use of BMI, calculated as BW/height 2 , has gained wide acceptance as a weight-stature index for use in diagnosing both protein-energy malnutrition and obesity ( 82,83,84). Most of the assumptions of weight -stature indices are fulfilled by BMI, although several limitations should be noted. First, although the correlation between BMI and TBF

is relatively strong (r = 0.5 to 0.8), individual variation is large and some subjects can be misclassified as undernourished or obese (81). For example, some athletic subjects have a large skeletal muscle mass and a high BMI but are not obese. Thus, man with a BMI of 27 can have TBF ranging from 10 to 31% of body weight ( 85). This variability in percentage of body fat may also increase in old age ( 86). In studies such as these, some of the observed error may be in the reference method for estimating body f at. BMI may also have a small stature dependence because persons with short legs for their height have higher BMI values independent of fatness ( 82). Finally, Gallagher and colleagues, using a four -component model as the criterion for body fat estimation, reported that BMI as a measure of fatness in their healthy cohort was age and sex dependent but independent of ethnicity in their African -American and white adults (87). Figure 49.4 shows how the relationship between BMI and body fat changes with age, as noted earlier. Generally accepted BMI ranges for classifying patients as normal, overweight, and obese are presented in Table 49.6 (88) (see also Appendix Tables A -13 and A-18 and their subdivisions). Table 49.6 also gives three BMI levels for grading chronic protein -energy malnutrition that are less well accepted (89). The diagnosis of protein -energy malnutrition or obesity and of their associated risks is often multifactorial and may require additional esti mates including body composition, energy expenditure, organ and tissue function, and biochemical markers.

Fat and Lean

Two methods are used to process anthropometric data other than body weight. The first method is to express the individual persons values relative to a healthy reference population. This method provides the anthropometric component used to assess whether and to what extent the patient is malnourished. The anthropometric reference tables present the results of large surveys and usually describe the general population. Reference data are now available for estimates from bioelectric impedance. The data in Appendix Tables A-15-e-1, 2, and 3 were adapted from Chumlea and associates and are based on data from the Third National Health and Nutrition Examination Survey (79). The estimates of TBW, percentage of fat, and FFM in these tables were derived from bioelectric resistance (R) measurements using standard prediction equations. TABLE 49.6. BODY MASS INDEX AND GRADES OF OBESITY AND PROTEIN -ENERGY MALNUTRITION

BODY MASS INDEX <16 GRADE Grade III protein-energy malnutrition

16.016.9

Grade II protein-energy malnutrition

17.018.5

Underweight (grade I protein -energy malnutrition)

18.524.9

Normal

2529.9

Overweight

3034.9

Class I obese

3539.9

Class II obese

>40

Class III severe obesity

P.766

The reference tables usually present data in three forms: (a) as a mean value; (b) as mean and standard deviation (SD); and (c) as percentiles. Describing a population in terms of mean and SD assumes that the measurement under study is symmetrically (norma lly) distributed. If data fit this model, then the mean 2 SD includes 95% of the population. An abnormal value is more than 2 SD above or below the mean. Some tables provide only a mean, and the patients value is then expressed as a percentage of the standard or reference value. A weakness of this approach is that tables of this type do not provide the observer with a method of determining whether the result is within the normal range. The second type of table includes the SD, or 95% range of the healthy population, thus indicating whether and to what degree the patients results are abnormal. The third mode of expression is in terms of percentiles (e.g., see Appendix Tables A -12 to A-16, and A18-b). The advantage of expressing results as a percentile rather than as a percentage of standard is that the

reference population need not be symmetrically distributed. Often anthropometric surveys of populations produce skewed distributions, and therefore the easiest option is to present results in percentiles (90). In this approach, the values of the subject exactly in the middle of the group are at the fiftieth percentile. If the patients value is b etween the fifth and the ninety -fifth percentile, the result is considered normal; a result below or above these respective values is abnormal. No simple method of judging the severity or potential morbidity of protein-energy malnutrition from anthropometric data is available. Studies in adults have not yet clearly defined the risk of a subnormal anthropometric index, especially for results falling just below the normal range. Combining anthropometric data with the results of other components of the nutr itional assessment provides some measure of potential morbidity ( 91). The second method of expressing anthropometric data is in terms of the individual persons total body energy content, TBF, and FFM. When estimated energy and nitrogen balance are combined with these body composition data, a whole spectrum of potential calculations is possible. Of course, these are approximations, but their appli cation in teaching and solving simple clinical questions often proves useful.

CLINICAL APPLICATIONS
Suggested applications of anthropometry are the following:

Weight and height should be recorded in the chart of every hospitalized patient. Weight indices, such as recent weight loss, should be added to the data base for all patients who have a history of weight change.

The weight of all patients undergoing short -term nutritional support should be measured daily.

The uses of one skinfold measurement, limb fat area, and limb muscle area are helpful:
o

When body weight is an invalid index of energy reserves because of edema or massive tumor burden. The upper limb is us ually not affected by dependent edema. When body weight is unmeasurable because of immobilizing devices, such as a cast or respirator. When patients are seen for nutritional consultation or are seen at rounds removed from the bedside. Anthropometric estimates provide a quantitative description of what is usually visible at the bedside. Although weight alone is useful in this regard, two patients of the same height and weight may differ in body composition. During the initial evaluation of hospitalized patients who are prescribed short -term nutritional support. Although changes in fat and lean tissue will most likely not be detected over a 1 - to 2week period, the baseline anthropometric data will become a permanent component of the nutritional data bas e. This information will then be available if a future reevaluation is needed.

TBF and FFM are useful indices:

o

In patients who are undergoing long -term nutritional follow -up over months or years. Limb muscle area measurements, preferably of the upper arm, should also be included in this group to complete the body composition data base.

In groups of subjects forming the basis of nutritional studies, when a more critical assessment of body composition is often useful and more accurate techniques of evaluating body composition are not available. In estimating RMR based on FFM. For teaching purposes, when the interrelations of metabolic balance, body composition, and nutritional therapy are the subject of discussion.

o o

AGING AND ANTHROPOMETRIC INDICES

Body composition changes throughout the adult life span, and this must be considered when evaluating anthropometric indices ( 92). Height declines and, assuming body weight remains unchanged, there is more fat and less FFM in an elderly person than in a younger one of the same sex (92,93,94). Most of the loss in FFM can be accounted for by a decrease in skeletal muscle ( 95). A summary of how body composition changes with age and how anthropomet ric measures are affected is presented in Table 49.7. Because of these changes in body size, shape, and composition of the FFM, investigators now advocate geriatric-specific anthropometric and bioimpedance body composition prediction equations ( 96,97,98). A difficult problem in the elderly is estimation of height, especially in wheelchair -bound, bedridden, or kyphotic P.767 persons. Specialized approaches such as recumbent anthropometry may be useful in hospitalized or nursing

home patients (99). Another useful approach is to measure knee height or arm span (see Table 49.2) to predict adult stature. Knee height and arm span undergo little change with age in adults and provide estimates of stature that are difficult to obtain by conventional methods. The estimated value for height can then be used in calculating other assessment indices and for comparison of these results to height-adjusted reference values. Alternatively, knee height can be used in place of stature in indices such as fat/knee height 2 (100). TABLE 49.7. EFFECTS OF AGING ON BODY COMPOSITION AND ANTHROPOMETRIC MEASUREMENTS

ANTHROPOMETRIC MEASUREMENT Weight AGE-EFFECT The average population value increases until the fifth decade and then plateaus or decline.

Height

The average population value decreases by 0.5 to 1.5 cm per decade after maturity; the rate of decline is sex and race dependent

Fat

Fat increases as a percentage of body weight up to about 50 y and then plateaus or declines in

old age after 70 y; redistribution occurs from limb to truncal subcutaneous sites and from subcutaneous to internal, visceral, and interstitial sites

FFM

FFM decreases after age 40 y owing to decreases in skeletal muscle and bone; rates of loss in muscle are higher in men and accelerate after age 70 y; rates of loss in bone are higher in women and accelerate during menopause; the mass of visceral organs decreases slightly in old age; the hydratio n of FFM becomes more variable

Skinfolds

The compressibility of skinfolds changes with age owing to a loss in elastic recoil of skin and an increase in the viscoelastic recovery time; skinfolds in the elderly are often pendulous and difficult to measure additionally owing to loss of underlying muscle tone

Circumferences

Pendulous skinfolds can make circumferences more difficult to measure in the elderly; it is more difficult to locate bony landmarks in the obese

FFM, fat-free mass.

Anthropometric measurements may be useful in diagnosing malnutrition in hospitalized elderly subjects. Lansey and colleagues examined 47 consecutive geriatric patients admitted to an acute care facility and found that approximately 45% of the patients had two anthropometric measures (i.e., midarm cir cumference and muscle area; subscapular and triceps skinfold) less than the fifth percentile, indicating severe malnutrition ( 101). In contrast, only 28% of patients were at less than 90% of ideal body weight. Anthropometric measurements may therefore supplement and be more sensitive than body weight and stature in the evaluation of malnutrition in hospitalized elderly patients. Anthropometric me asures may also predict disability and mortality in elderly populations. Rolland and associates reported that the simple measurement of calf circumference predicted self-reported disability in a population of elderly women (102). Campbell and colleagues reported that low arm muscle area and triceps skinfold thickness were associated with significantly increased mortality risk in 758 subjects who were more than 70 years old ( 103). The MiniNutritional Assessment, which is now widely used to screen

elderly patients for malnutrition, incor porates midarm and calf circumferences and BMI (104).

EVALUATING AND CONTROLLING ERROR SOURCES

As with all measurements, anthropometric evaluations include error. In this section, we provide an introductory discussion on anthropometric error sources. The interested reader is referred to comprehensive reviews for an advanced discussion of this important topic ( 8,20,22). Error can be considered in the context of the fundamental body composition methodology equation as shown in Figure 49.8. The equation in the figure indicates that P.768 error in the estimation of a body composition component (e.g., TBF) from anthropometric measurements is a function of two main errors sources, measurement of a quantity (Q) and mathematic function (i.e., descriptive or mechanistic). The figure also notes that errors of measurement may be either or both systematic (nonrandom) and random. Errors resulting from misspecification of mathematical functions are always systematic . The following discussion first considers measurable quantity errors and then proceeds to an overview of mathematic function errors.

Figure 49.8. Sources of error in anthropometric methods. A subjects anthropometric dimensions can be evaluated at a single point in time or on repeated occasions over time. Measurement error is the main concern with a single evaluation and measurement error combined with normal biologic variation must be considered with repeated measurements. Measurement error can be ca used by instrument error and observer error. Methods of minimizing instrument error are reviewed in earlier sections. In summary, these mainly resolve to the correct choice of appropriate measurement instruments and accurate calibration. Observer error is related to three factors: precision, reliability, and accuracy. Accuracy is the level of agreement between the measured value and the true dimension. Accuracy of an anthropometric dimension is usually established by comparison to a reference method. For example, subcutaneous adipose tissue thickness estimated using a skinfold caliper can be compared with corresponding

estimates by computed tomography or magnetic resonance imaging. Of course, any such analysis also includes instrument and observer errors. In clinical situations, measurements by an anthropometrist are usually compared with those of a designated expert ( 20). Precision, as distinct from accuracy, defines the quality of a measurement in terms of being sharply defined or exact. In this sense, precision refers to the scale of measurement; for example, a skinfold measured to the nearest 1 mm is more precise than one measured to the near est 0.5 cm. A highly precise measurement (e.g., body weight measured to the nearest gram) is not necessarily accurate if the weight scale used is improperly calibrated. The definition of precision overlaps to some extent with that of reliability. Reliabili ty is the degree to which a measurement is replicable using the same instrument by the same or a different observer ( 105). The linkage to precision comes in that it is difficult for a measurement to be precise or exact if it is unreliable. The precision of an anthropometric measurement can be quantified as the variability among repeated measurements over a short time in the same subject ( 22). One way of expressing precision is the technical error of measurement, which is the standard deviation of repeated measurements on the same subject by the same or different observers. The technical error of measurement, which is expressed in the same units as the measured quantity, can also be expressed in percent as a coefficient of variation (i.e., SD/mean 100) (20). Reliability is also referred to as reproducibility or repeatability (105). Reliability, as distinct from precision, is more commonly expressed in terms of the intraclass correlation among repeated measurements, sometimes

called the reliability coefficient. Measures of reliability often include both measur ement error and physiologic variation. The total variation of an anthropometric measurement monitored over time includes measurement variation and biologic variation. Biologic variation occurs even in the healthy person as weight and fluid balance fluctuat e over time. This aspect of measurement variability is the difference between total anthropometric dimension variation over time and that caused by measurement error. Some measures, such as stature, are extremely stable in adults, whereas others, such as s elected skinfold thicknesses, are moderately variable over time. In practice, this biologic component of variability is often included in estimates of the reliability on anthropometric measurements. Anthropometric dimensions are often used directly, as for example triceps skinfold thickness as a measure of fatness. Mathematically transforming an anthropometric measurement to a component estimate involves error sources. The validity of an anthropometric method in this context is the degree to which it accura tely measures or predicts a specific component. Descriptive or type I methods are population specific, and error may arise when applying the prediction formula to a new subject group or outside the original subject range for age, weight, and stature. Mechanistic or type II methods include model error. For example, calculation of arm muscle area from triceps skinfold and midarm circumference is based on a simple geometric model. Actual arm muscle area may deviate from the assumed model, and this introduces e rror into the component estimate. Both types of error are nonrandom or systematic.

Anthropometry is applied widely in evaluating a single subject or whole populations. Professionals who apply anthropometry in their clinical work or research should fully comprehend the nature of anthropometric error sources and apply procedures to maximize the quality of their measurements. A good policy is to set up an evaluation program for the anthropometrists ( 20). An approach such as suggested in these reports will help to maintain a high quality measurement standard.

CONCLUSION
Anthropometry is one of the oldest approaches to quantifying body composition, and it is the most practical to apply in field and clinical settings. The severity, response to nutritional treatment, and aspects of subject malnutrition risk can be established using relatively simple and easily acquired anthropometric measurements. For thes e reasons, anthropometry is an indispensable tool for the practitioner of clinical nutrition.
1

Abbreviations

BCM body cell mass BIA bioimpedance analysis BMI body mass index Db body density DXA dual-energy x-ray absorptiometry FFM fat-free mass

R bioelectric resistance RMR resting metabolic rate TBF total body fat TBW total body water P.769

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