COMMITTEE ON NUTRITION

METHODS FOR DETERMININGCOMPOSITION OFTHE HUMAN BODY

With a Note on the Effect of Diet onBody CompositionGilbert B. Forbes, M.D.

Department of Pediatrics, University of Rochester School of Medicine and Dentistry,Rochester, New York

born and adult are presented in Table I,both on a fresh-weight and a fat-free freshweight basis. The latter basis for expressing values avoids discrepancies that arisebecause of alterations in fat content. It isevident that signfficant changes in bodycomposition occur during growth. Water,sodium, and chloride contents decline,while contents of nitrogen, calcium, potassium, magnesium and phosphorus all increase. In these data, body fat content isnot strikingly different in the two agegroups. As will be discussed later, measurements on living subjects reveal an increasing adiposity in later adult life.

The extensive observations of Widdowson and her@ @‘¿�12 have shownthat growth changes occur in body composition of other mammalian species, changesthat are comparable in magnitude and direction to those of the human. These species include the mouse, rat, cat, guinea pig,rabbit, and pig. It is entirely probable,therefore, that the trend of changes in bodycomposition depicted in Table I representsa phenomenon common to all mammalianprotoplasm.

In considering the data of Table I, it isevident that some variation is present, evenwhen the values are calculated on a fat-freebasis. Sources of variation include losses ofelectrolyte when tissue specimens areashed, technical difficulties in analyzing

T HE EARLY NINETEENTH CENTURY wit

nessed the first concerted application ofchemical techniques to the investigation ofbiologic materials. Milk was chemicallyanalyzed, von Liebig discovered the chemical contrast between potassium-rich cellsand sodium-rich tissue fluids, and CarlSchmidt analyzed blood serum in great detail. Soon these methods were applied tothe study of the entire human body.

The advent of isotopic dilution techniques in the 1930's and 1940's broughtabout a renewed interest in body composition. More recently these and other techniques have been used in an attempt tostudy the nutritional aspects of body composition. It is the purpose of this report topresent the various methods now in use andto discuss the virtues and limitations ofeach.

DIRECT CHEMICAL ANALYSIS

Whole Body

During the past century a number of human carcasses have been analyzed for water, fat, nitrogen, sodium, potassium, chloride, calcium, magnesium, and phosphorus.These include the fetus, newborn, andadult. The few analyses done on childrenhave included subjects suffering from conditions known to profoundly affect waterand electrolyte metabolism.

Data for total body content in the new

Supported by grants from U. S. Atomic Energy Commission, Contract No. AT (30-1)-1827 with theUniversityof Rochester,and U. S. Public Health ServiceNo. A-1406.

ADDRESS: 260 CrittendenBoulevard, Rochester20, New York.

PEDIATRICS,March 1962

477

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SubjectsPer

ce,@Imeq/kg

Na Cl Kgm/kgReferencesCa P————Mg1120FatNitrogenTotal

WeightBasisNewborn3

(8)(av LS@O gin)7@ (69—73)11(10-16)1.97 (1.8—I@t)7$

.50 40(07-81) (4S—5@) (36-43)7.1

4.5(5-9.3) (3.4—5.3)0.

17(O.1—.@t)Camerer

&Söldner'Newborn,i

(6)(av 3.560 gm)69161 (1I—@8)1.90(1.7—@.@)SQ

. . 44(77-87) (39-47)8.0

4.7(7.4—8.9) (4.3—3.1)O.Q@(O.19—@t4)\@iddowson―@Adults84

(39-68).

.. .. . . . . .. . . ...OlderGermanIiterature@Adult

remale.56@42.3074 . . 5619 9.90.33Subject “¿�L―W'iddowson ciat.'Adult

male68IC@.SI. - . - - -16 7.7. .Mitchell ciat.'Aduitmale35181.9868

36 5419 9.@..f

@R.M.ForLas@ta1.@ ‘¿�(J. II. Forbes andLewis'Adultmale3@e7v.7637

40 49168.@033Adult

male71• 43.16. - - - . -@OII0.45Averages6@17@.7O66

38 53189.10.38Pal-free

WeightBasisNewborns

(av@8I0gm)81.9 ±0.7..@@t3 ±0.138$.l

56.6 46.0±8.6 ±4.6 ±@.98.@3

5.09±1.34 ±0.670.19±0.01(1)Newborns

(av3,S6Ogin)8@.3..Q.Q6 ±0.1698.St.. 5@.1

±3.0 ±@.69.335.37

±0.69 ±0.310.@6±0.&t(@,3)Adults7@.4

±3.7..3.@8 ±0. 4685.849.8 68.6

(78-96) (44—56)@66—73)@I.711_i

±@ .5 ±I .50.46(.43—48)(4,5,6,7.8,9)Adults71.1.

.3.6647.7 41@t 66.8eo.i 11.60.36Shohl'°

478 BODY COMPOSITION

TABLE I

TOTAL BODY C0MI0SITI0N8

S Variations e@pressee1 either as range or standard deviation.

t Widdowson's'-' series included one large subject (4,375) gm) containing @8.3%fat by analysis. The distribution of values for fat contentis thus skewed. This subject also contained a large amount of sodium (108 meq/kg fat-free weight), though other constituents were normal.

Average values for the remaining five subjects are fat 13.6% (range 11—15),and sodium 96.3± 1.9 meq/kg.

bone for sodium, chloride, and magnesium,and the fact that the subjects are not all ofthe same age and weight. These factorsmay account for the lower values for Na, K,Ca, P, and Mg in Camerer and Söldner'sstudy of newborn infants in comparison toWiddowson's results. For example, theformer group of subjects weighed less(2,480-3,350 gm) than the latter (3,050-4,375gm). The low value for Na reported in theadult by Shohl1° and the high value reported by Widdowson et al.' are unexplained; the former differs so much fromthose reported by other workers that analytic error seems likely.

Perhaps the most serious source of errorlies in the fact that some, or perhaps all, of

the subjects are not representative of thenormal population. The obvious fact thatdeath occurred raises the distinct possibility of chemical derangement.

Individual Tissues

A number of individual tissues have alsobeen studied. During growth the concentrations of water, sodium, and chloride inmuscle and brain decline while that of potassium increases.1316 Of interest is the factthat this trend is reversed, though to a veryslight degree, in ageing rat muscle.' In experimental malnutrition, the infantile typeof chemical pattern in muscle tends to persist.18 Bone differs from most soft tissuesin that sodium content increases during

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REPORT OF COMMITTEE ON NUTRITION 479

growth, as does the content of calcium,phosphorus, and magnesium, though watercontent does diminish.192' The value ofbiopsy specimens in assessing nutritionalstatus is somewhat limited except in instances of severe malnutrition,15 or wheredefinite metabolic abnormalities exist. Biopsy analysis provides information on the tissue concentration, not on total body content.

INDIRECT MEASUREMENTS OF WATERAND ELECTROLYTES

Obviously chemical analysis must be limited to biopsy specimens in living subjects.In recent years, a number of indirect methods have been devised for the estimation ofcertain aspects of body composition in man.

Isotopic Dilution Technique

The ready availability of stable and isotopic tracers at the end of the war stimulated investigation of total body composition in living man. Methods for estimationof total body water and total exchangeablesodium, potassium, and chloride have beendeveloped and used extensively in both normal and diseased subjects.

In general the technique consists in administering a known quantity of tracer andallowing a period of time to elapse for mixing of administered tracer with non-tracerpresent in the body. Urine is collectedquantitatively during this period, at the endof which a sample of serum is obtained foranalysis. If tracer is designated as X°,andnon-tracer as X, then

total exchangeable X =

X@ administered —¿�X* excreted

serum X°/serum X

Now if the ratio of serum X°/serum Xis equal to whole body ratio of X°/X, totalexchangeable X will be identical withwhole body content. Fecal and cutaneouslosses of X° are usually negligible. Thetime allowed for mixing has usually been]to 3 hours for deuterium oxide or tritiumoxide, 4 to 24 hours for stable bromide orradiobromide, 18 to 24 hours for radiosodium, and 24 to 40 hours for radiopotas

sium. Bromide is substituted for chloride,since there is no convenient isotope of thelatter. Antipyrine, or one of its derivatives,may be substituted for deuterium or tntium. Fniis-Hansen et al.22 found, in a seriesof infants and children, that the volume ofdistribution of deuterium was 2% higherthan that of antipynine.

Although there is considerable evidencethat the results of isotopic dilution measurements do approximate total body contentin small laboratory 2324 data forhuman beings must be qualified to a certainextent. Deutenium and tnitium oxides mixwith tissue water very rapidly, and there isin addition some exchange with nonaqueous hydrogen, leading to an overestimationof 0.5 to 4%. For bromide, sodium, and potassium, mixing is slow and often incomplete in the case of erythrocytes and centralnervous system tissue, and very slow in thecase of sodium in bone.

In the adult, it appears that the dilutionmethod yields appropriate values forwater,2' subject, of course, to the possiblesmall discrepancy previously mentioned.The situation is not so clear in the case ofthe other isotopes : The ratio of total exchangeable content to actual content is 0.85to 0.97 for potassium and chloride andabout 0.7 for sodium.9@2628 In the newborninfant correspondence is good for chlorideand water and fairly good for sodium andpotassium.2932

Of current interest is the amount of radiation delivered to the body during theseprocedures. For the short-lived isotopes,

such as K42, Na24, and Br82, and for tritium,the total dose is usually less than 0.2 roentgen-equivalent. Deuterium is of no concernsince it is a stable isotope. Long-lived sodium (Na22-physical half-life 3 years) presents a potential problem. Although mostof the isotope is eliminated from the bodyof the adult with a biologic half-time of 11days, a small fraction (less than 1%) is discharged very slowly with a hall-time ofabout a ar33'34 Because of the very slowdisappearance rate, this minute fraction accounts for as much as 10%of the total radia

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480 BODY COMPOSITION

tion dose. Presumably this slow componentis in bone. °No data are available on thebiologic half-life of Na22 in infants.

Whole Body Radiation Counter

In recent years, instruments have beenconstructed by which the minute amountsof radiation emanating from the body canbe accurately measured.35 This radiationarises from naturally-occurring radioactiveelements ingested in food and water, andalso from fall-out by-products of the atomicbomb explosions. Indeed, these instrumentsare now being used to assess certain aspectsof the magnitude of the radioactive fall-outproblem.

Of interest to the present discussion isthe fact that the body content of potassiumcan be measured in this 636,37 Threeisotopes of potassium exist in nature, andone of these (K40) is radioactive, with a physical half-life of 4 X i0@ years. Potassium4°constitutes 0.012% of total naturally-occurring potassium. Thus, an estimate of theamount of potassium present in the bodycan be obtained by measuring its K4°content. Since the human body contains verysmall amounts of K4°(about 102 @&c)themeasuring device must be unusually sensitive. Due to the extensive investigationsof Anderson, Langham, and co-workers26―6with the Los Alamos whole body counter,we now have more complete data on potassium content in man than for any otherconstituent. Some 1,600 people have beenstudied by these authors.

Figure 1 depicts the changes that takeplace in water, potassium, and chloridecontents of the human body during fetaland postnatal life. These are the only constituents that have been studied systematically and in detail. (Total exchangeablesodium has been so studied, but this doesnot have a precise relationship to total bodycontent.)

0 The combination of these two factors results

in a somewhat greater radiation dose than is thecase for the other isotopes. Although a precisefigure for skeletal dosage cannot be given at pres

ent, it is unlikely that this exceeds current tolerancelimits.

Water content declines progressivelythroughout fetal life and early infancy. Recent data42 show that sex differences become apparent by 4 to 7 months of age. Atthis time the male/female ratio for bodywater is 1.04, on a per kilogram basis. Atadolescence the sex difference becomesmore evident, and there are wide differences between male and female adults, presumably because of differences in fat content. The decline in total body water duringageing also may reflect alterations in theamount of fat.

Total body chlaride shows a similar trendas growth proceeds. Sex differences appearearly in life (male/female ratio being 1.11by 4 to 7 months of age42) and are quitepronounced in early adult life. Admittedly,the isotopic dilution procedure may underestimate total body chloride by about 10%in the adult, but the general trend withage is nevertheless clear.

Potassium, on the other hand, shows asteady rise throughout the fetal and childhood periods. Sex differences, in the dataavailable thus far, first become clearly apparent early in the second decade. Maximum values occur here, after which thereis a gradual and progressive fall possiblyreflecting, as in the case of total bodywater, an increasing adiposity. Some variation does occur within each age group, thestandard deviations being about 10 to 15%of the means.

Fat content, as determined by chemicalanalysis, is of the order of 0.5 to 1%in earlyfetal life, increases slowly at first, and thenvery rapidly in the last trimester.3 Widdowson found that total body fat in the humannewborn (12-16%) was higher than that ofany of the other mammals she studied, including the guinea pig.

Data on total body fat in postnatal lifewill be presented in a subsequent sectionof this memorandum.

Again referring to Widdowson's studieson body composition in mammals, and toHamilton's47 data on the rat fetus, thechanges illustrated in Figure 1 for man areduplicated in other species. This intenspe

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REPORT OF COMMITTEE ON NUTRITION 481

c@

I,

S

. Wotsr

:@

Fic. 1. Total body content of H@O,Cl, and K in relation to age. Each point representsan average of several subjects. Symbols as follows: H@O and K—combined sexes •¿�,males •¿�, females •¿�; Cl—combined sexes •¿�, males@ , females@ . Data for fetusand newborn are from Kelly et al.― and ?3 Data for infants, children and

adults are from the following sources : Water (deuterium or tntium dilution)—Friis-Han

son,39 Edelman et al.,@ Prentice et al.,@°Gilder et al.,4' and Owen et al.;42 potassium(K―counting)—Andersonand 3643chloride (Br'2 or stable Br dilution)—Forbeset ci.,― Cheek― Ikkos et al.,° and Owen et al.42 One set of values has been omitted,

namely, that for the 3-month fetus analyzed by lob and Swanson.@' Although water con

tent was in keeping with the general trend, low values for Cl (21 meq/kg) and K (9meq/kg) were reported. The reason for these seemingly aberrant values is not clear.

U IChloride

S@@ 0 0

Potassium

•¿�0

@E,YEARS

cies correspondence is manifest not only inthe direction of the change but also in therate at which the changes occur at differentperiods of growth. The decline in water andchloride contents, and the increase in potassium content, are most rapid in early life,when growth is rapid; during later periodsof decreased velocity of growth, changesin composition proceed more slowly. Moulton,48 impressed by the rapidity of compositional change in early life, announced in1923 his theory of “¿�chemicalmaturity.― Thistheory states that at a certain time in the

life of animals and men, body composition(fat-freebasis)attainsitsadultvalue,whereit then remains. Close inspection of his data

reveals that composition does changeslightly after this point is reached, but tomuch less a degree than in early life. Aswill be discussed later, changes in fatcontent continue to occur throughout mostof adult life.

Changes in contents of water, potassium,and chloride appear comparable duringgrowth in all mammalian species studiedthus far. This is best demonstrated by the

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482 BODY COMPOSITION

allometric method whereby plots of log

body content against log weight yield aseries of straight lines.@@ The resultingslopes, which really represent percentageincrements of chemical growth, show a remarkable interspecies correspondence. Therelative rate of change in body composition, as well as its direction, would thus appear to be independent of species; this ratemay also reflect a fundamental property ofmaturing mammalian protoplasm.

The trends in body content of chlorideand potassium illustrated in Figure 1 alsoserve to define approximately the changes

in volumes of extracellular and intracellu

lar fluid occurring during growth. The dataof Friis-Hansen39 indicate that extracellularfluid accounts for about 70% of total bodywater in the 5-to-6-month fetus, 55 to 60%in the newborn infant, 44% in the one-yearold child, and 33% in the 3-to-16-year-oldgroup. The magnitude of the extracellularfluid compartment (and of intracellularfluid, since this is calculated by subtraction)varies with the method used for its determination. Friis-Hansen used thiosuif ate;others have used inulin, thiocyanate, bromide, and, of course, chloride.

Cheek5° has recently reviewed the subject of extracellular fluid and its measurement. This fluid compartment has beendifficult to define anatomically; there hasbeen much argument as to whether itshould be considered to include cerebrospinal and joint fluids, and the fluid withinthe gut. No substance has yet been foundthat will leave the vascular compartmentquickly after injection and yet be constrained from entering certain tissue cells,and it is doubtful that such a substancewill be found. The extracellular fluid is theprincipal avenue connecting body cells withthe outside world; it follows that a greatmany substances must be continually leaving and entering it at a very rapid rate. Itit unlikely that the volume of distribution ofany substance would coincide with thisvery active body fluid compartment.

One further consideration has beenraised by the recent experiments of Peter

son et 5@These authors measured extracellular fluid volume by the constant infusion technique (sucrose) over a period of

10 to 24 hours in a number of subjects.They found that rather large variations incalculated volume of extracellular fluid occurred in each of the subjects, the coefficient of variation averaging 8%. Only aboutone-fourth of this variation could he ac

counted for by technical errors; the authorsconsequently concluded that physiologicshifts in body fluids are continually takingplace.

Quantitative Roentgenography of theSkeleton

Suggestions have been made from time totime that this method could be applied tothe assessment of body calcium stores. It iswell established that 99% or more of thetotal body calcium is in bone, and Macket al.52 have calculated that about 80% ofthe total x-ray absorption by bone is dueto the calcium present therein. A recentstudy has shown that the bones of malnourished Indian boys are less dense thanthose of American boys.5@

Schraer5' has recorded estimates of bonedensity (os calcis and phalanx) for children

of both sexes between the ages of 7 and 20years. A gradual increase in density occurs

over this period. For the phalanx, densityis higher in the female, while the reverse is

true for the Os calcis. Differences of 15% or

more in bone mineralization can be detected by this method.55 Mainland56 has defined the multiple sources of error (soft tissue masking, irregular contour of bone, filmposition and processing, etc.) which are inherent in the roentgenographic technique.Barnett and Nordin'T have suggested the

simpler technique of using the cortex/shaftratio in femur and degree of biconcavity ofvertebrae to assess the degree of osteoporosis.

ESTIMATION OF TOTAL BODY FATA number of methods for estimating

total body fat have been tried. Some aredesigned to provide absolute values, while

others can only yield comparative data.

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REPORT OF COMMITTEE ON NUTRITION 483

Brozek,' an estimate of total body fat canbe obtained.

Body density is usually determined in tileadult by weighing the subject in air andimmersed in water, with appropriate corrections for residual air in lung and intestine. Zook'2 succeeded in measuring specificgravity in a group of 5-to-19-year-old boys,and ParIzková6' has published values fordensity of 9-to-17-year-olds of both sexes.The former article includes a bibliographyof the older literature on specific gravity.

Body volume of adult human subjects hasbeen determined by Sin64 employing amethod of helium displacement, and themethod of air displacement has been usedfor animals.65 If body volume is known,density can be calculated and an estimate

of fat made.Several difficulties present themselves in

the use of the densitometnc method forestimating body content of fat. The actualtechnique of measurement is rather difficult.In addition, the density of the lean bodymass has never been measured directly, the

value used being derived from data for individual tissues. For the infant and child,this value undoubtedly differs from thatof the adult.

For both densitometric and total bodywater methods, as originally used, the assumption is made that the lean body masshas a constant composition. This assumption receives support from studies on smallanimals, particularly those of Rathbunet al.@6More recent tu768 of a varietyof isolated human tissues reveal that bothdensity and water content can be related tofat content.

If both methods are valid, they shouldyield comparable results. Osserman et al.69found that this was indeed the case. Behnkeand Sin,70 on the other hand, in studyinga series of 31 young men, found an averagefat content of 22% by total body water and18% by densitometry. In a series of youngwomen, Young et al.?1 found an average fatcontent of 28% by total body water and 25-29% by densitometry, depending on the particular formula used for calculation. Tan

Total Body Water Method

If it is assumed that the fat-free body orlean body mass (LBM) has a constant watercontent, and that neutral fat is stored dry,it becomes possible to calculate total bodyfat from the water content of the body.Since lean body mass of the adult contains72% water,

total body water (kg)LBM (kg) = _______________

Total fat is then body weight minus leanbody mass.

In the newborn infant the denominatorshould be 0.82, for this is the water contentof the lean body mass in this age group(TableI). Nodatafromcarcassanalysisareat hand for the older infant and child, andit is not known when the transition between

infantile and adult body composition iscomplete. Moulton48 has suggested that thisis accomplished at about age 3 years.

The validity of the calculation dependson the constancy of composition of leanbody mass. The few chemical analyses donein adult man, and the many carried out inanimals, support this contention, but extremely obese human subjects have notbeen analyzed. tu5@9 on obese subjects before and after weight reduction re

veal that the tissue lost by these patientscan be calculated to contain 15% water and

23 meq of potassium per kilogram; if thisbe the case, either the water content of thelean body mass changed during weightreduction, or lean tissue was lost in additionto fat.

Densitometric Method

Since fat has lower density than leantissue, Behnke et al.60 proposed that fat con

tent could be estimated from a measurement of the density of the whole body. Thenearer this figure is to the density of fat(0.901) the fatter the subject, and thosesubjects whose density approaches that assumed for the lean body (1.097) are obviously quite lean. By using an appropriateformula, such as the one given by Keys and

0.72

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484 BODY COMPOSITION

ner72 pointed out that any lack of correspondence between these two methodsmust inevitably result in a certain error inestimation of fat, and that this error isappreciable.

Is the concept of a constant “¿�leanbody

mass,―to which fat is added to a greater extent in the obese than in the normal, avalid concept, or is it merely a convenientabstraction? The fact that individual tissuesamples show a high degree of constancywhen composition is calculated on a fatfree basis does not allow one to assumecategorically that the total lean body massdoes not change as fat is added to or subtracted from the organism. Keys and Brozekol reported that the density of the tissueactually gained or lost under controlledconditions in man is 0.93 to 0.95 (purefat = 0.90) and that the calculated composition of this tissue is 64% fat, 23% cellularmatter, and 13%extracellular fluid.

In the light of these findings, a new concept has arisen, namely, the “¿�standardreference man,―containing 14% fat, 61% water,19% protein, and 6% minerals. A given adultsubject differs from this hypothetical mdividual only in having a different proportionof adipose tissue, which is assumed to be62% fat, 31% water, and 7% protein. Keysand Brozek6' have derived a formula basedon this concept for calculating fat content.

Ljunggren and@ proposed avariation of this concept, in which the bodyis divided into “¿�obesitytissue― consistingof fat and its supporting connective tissue,and “¿�non-obesitytissue― which is the remainder of the lean body mass. “¿�Obesitytissue―is considered the main variable affecting body composition.6

Sin74 has proposed a new formula, whichembodies values for both density and bodywater. With both of these parameters athand, the resultant calculation for body fat

0 Analysis of 12 samples of adipose tissue from

exsanguinated rat, dog, and rabbit revealed 41 to93% fat (average 80%); on a fat-free basis watercontent was rather uniform (81%); sodium, chloride,

and potassium concentrations were 122, 134, and68 meq/l of water, respectively.―

is not affected by variations in tissue hydration, since the assumption of compositionalconstancy of the hydrated lean body massis no longer necessary. However it is stillnecessary to assume a constant ratio ofmineral/protein in the body, in other wordsa constant density for lean body solids.

The investigator today is thus faced withthe problem, once the density measurementhas been made, of deciding which of 5everal formulas now available should be usedin deriving a value for actual fat content.Although body density can be measuredwith precision (standard error O.2%@')calculated fat content will vary with particularformula employed. In the study of Younget al.,71 employing five different formulas,

calculated fat content varied from 25 to29%. Lim and Luft76 studied a group of maleadults. The Sin formula yielded results forfat content some 6 to 7% higher than didthe Keys-Brozek formula. Taking 20% foraverage fat content, this means that the discrepancy between the two methods of calculation is of the order of 30%. One canhardly disagree, therefore, with Lim andLuft's conclusion that “¿�thetrue values forbody fat cannot be stated with certainty atthe present time.―

The matter of relative size of the skeleton(e.g., the “¿�small,―“¿�medium,―and“¿�large―frame referred to in weight tables fc.adults) presents another difficulty for boththe densitometric and body water methods.The existence of this variable is evidentfrom the data on calcium (Table I). Sincethe skeleton has a much lower water content and a much higher density than softtissues, it is evident that variations in skeletal size would alter both density and watercontent of the lean body mass. Despite allof these objections, both the densitometricand total body water methods are currentlyin use as a first approximation of fat contentof the adult. It is reported that certainphysiologic phenomena, such as basal metabolism and cardiac output, correlate betterwith fat-free weight than total weight orsurface area.'6 Such little use of these methods has been made in childhood that anevaluation cannot be made at this time.

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REPORT OF COMMITTEE ON NUTRITION 485

Creatinine Coefficient

A number of years ago Talbot7@ proposedthe use of the creatinine coefficient (creatinme excretion expressed as mg/kg/24 hr) asan index of obesity. He found this value tobe inversely proportional to the degree ofobesity as judged by weight and clinical criteria.@ have determined this coefficient in infants and children of variousages. The coefficient is higher in adolescentboys than girls; this and other observations

have led to the contention that creatinineexcretion is proportional to the muscle massof the body. Recently Talso et al.27 andMuldowney et al.8°found a high correlationbetween creatinine excretion and total body

potassium (r 0.8 —¿�0.9); Miller and Blyth8'found a high correlation between densitometrically determined lean body mass andcreatinine excretion in adults. Kumar et al.82have related creatinine excretion to chemically determined lean body mass in rats,but pointed out the need for using a lowcreatinine diet and a urine collection periodof at least 48 hours for accurate results.

The situation in the young infant is notso clear. The data of Catherwood andStearns8@ indicate a good correlation between creatinine excretion and body weight

in full-term infants. Cranny and Cranny,84on the other hand, found large variationsamong premature infants, with a range ofas much as fivefold in infants of comparable weight. Kennedy's85 recent study ofhospitalized children revealed a rather poorcorrelation between creatinine excretion andtotal exchangeable potassium.

The creatinine method offers the obviousadvantage of ready availability, withoutthe need for elaborate technical procedures,though some workers have failed to followthe precautions suggested by Kumar et al.82From the biochemical point of view, creatmine production and excretion is far froma simple process, making it unlikely thatthe size of the lean body mass is the onlyfactor which determines excretion rate.

Measurement of Subcutaneous Fat Layer

known, it is likely that a considerable proportion of the adipose tissue of the body islocated subcutaneously.* Two methods forestimating subcutaneous fat have been usedin man: measurement of skinfold thickness(skin plus subcutaneoustissue)and softtissue roentgenography. Garn8T has reported that the two methods yield comparable results. For the former method,special calipers are needed—calipers designed in such a way that constant pressureis exerted at all jaw widths. The skinfoldmethod can provide information about therelative distribution of subcutaneous fatfrom region to region whereas the densitometric and body water methods give anestimate of total amount of body fat.

In the adult male, Brozek and associ89 and Pascale et al.9° have reported

a high degree of correlation between theskinfold and densitometric methods. Skinfold thickness increases with weight and iscorrelated with densitometrically determined fat content in adult@Forbes et al.92 found that skinfold thicknesscould be correlated with fat content asdetermined by K4°content. It would appearthat this relatively simple measurementcould serve as an index of obesity, at leastin the adult.

The studies of Stuart and Sobel,°3Garn°4Reynolds and Grote,95 and Pett and Ogilvie96 reveal that subcutaneous tissue thickness varies during infancy and childhood.Maximal values occur at about one year ofage, and in adolescence, and there is asteady increase during the adult years. Sexdifferences become apparent in early childhood.

In the recent flurry of concern aboutadiposity in the modern adult, many havefailed to appreciate the fact that the human

0 Analysis of one full-term newborn infant (fat

content 14%of body weight) revealed that 42% ofthe body fat was located subcutaneously.― In theguinea pig, subcutaneous fat makes up 12%of totalbody fat in males, and 20%in females; the relativeproportion of total body fat present in this site doesnot vary appreciably with the degree of fathess ofthe animal.―Although the precise fraction is not

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486 BODY COMPOSITION

infant is also fat. Indeed, subcutaneous tissue thickness in certain areas of the bodyexceeds that of the adult male. This is wellillustrated by the data of Pett and Ogilvie96obtained from a random sample of the Canadian population (Fig. 2). Obviously the

5-mm triceps skinfold thickness in the 2-year-old represents a far greater relativeproportion of subcutaneous fat than doesthe 4-mm layer in the 40-year-old male, orfor that matter, the 8-mm layer in the female.

The technique involved in making thesemeasurements is discussed by Keys andBrozek6' and Tanner.―

Use of Fat-soluble Indicators

A number of inert gases are much moresoluble in fat than in lean tissue. Thus thevolume of distribution of such substanceswithin the body should logically be a function of total fat content. Lesser et 998have recently extended their earlier workon cyclopropane absorption in animals to

a,.0 •¿�@

0 •¿�

00 00 @0

include human adults. This gas is 34 timesmore soluble in fat than in lean tissue. Resuits obtained in study of four male and twofemale subjects indicated values for fatcontent which were, on the average, 12%lower than those derived by the total bodywater method. Since the theoretic basisfor the cyclopmopane method is sound, thisdiscrepancy does not necessarily lead to itsinvalidation.

The procedure is time-consuming andtechnically difficult. Equilibration is not yetcomplete in 8 hours, so repeated analysesof the inspired gas and a complicatedmathematic treatment are necessary inorder to obtain an answer.

Radiokrypton has also been suggested,@°though no extended series of observationshas been reported. This method suffersfrom the same technical difficulties as thecyclopropane method, and introduces theadded feature of radioactivity. Behnke,10°noting the fact that nitrogen is five timesmore soluble in fat than in water, estimated

4+

0000

+ +

000

4 FsmaIs

4

+

0 oMals

0

0

DATA of PETT and OGILVIE

I@ .@@ I@ .@ , I .@ .@ I . . . . I .@@ . I@@@@ I@ I@ . .5 15 25 35

YsarsFic. 2. Average skinfold thickness as a function of age and sex, from the Canadian survey of Pett and

Ogilvie.―The measurement includes a double layer of skin plus subcutaneous tissue.

IIS@

•¿�THcepsSkinfold(mm@

IC

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body fat by measuring the amount of nitrogen washed out of the body during 12hours of breathing pure oxygen.

These methods offer considerable theo. retic advantage over those discussed pre

viously in that they constitute a direct,rather than an indirect, method of estimating fat content. It is unfortunate that theyinvolve such an intricate technique.

Total Body Potassium Method

On the assumption that the lean bodymass has a constant potassium content, andthat neutral fat does not bind electrolyte, itshould be possible to estimate total body fatfrom the potassium content of the body.Evidence from chemical analyses29@h1@12supports the contention that the adult leanbody mass has a relatively constant potas

REPORT OF COMMITTEE ON NUTRITION 487

sium content in both man and animals,though the values vary from one species toanother. Kuiwich et al.I@1found a high correlation between K4°activity and leanweight in meat samples. Several investigators26'27‘¿�@ a::have proposed that this methodcould be used as an index of body fat cantent.

The potassium content of the body can be

measured in two ways: by the K42 dilutiontechnique, or in the whole body scintillationcounter. The calculation of fat content ismade in a manner analogous to that employing total body water, namely,

total K content

concentration of K per kg of LBM

Figure 3 is a graph of percentages of fatagainst age, calculated in this manner from

LBM

I I

x females

I

xl@

I

40

20

L@ I@ I I10 20 30 40 50

AGE IN YEARSFIG. 3. Average percentages of fat in the body as a function of age and sex, calculated from the K―data

of Allen, Anderson, and Langham.―“¿�‘“¿�The curves bear a rough similarity to those of Figure 2.

. males

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488 BODY COMPOSITION

the extensive data of Allen, Anderson and2636, 43 It is of interest that ParIz

ková's study63 of body density in childrenyielded results comparable to those depictedin Figure 3, such as a clear cut sex difference, and a rapid rise in body density (andhence a fall in fat content) in the 15-to-16-year-old male.

The K42 dilution method may underestimate true potassium content to a certainextent. Reported values are 85%,2895%26and97%27 of those determined by whole body

counting in the adult. Comparison withvalues from carcass analysis yields a figureof 85% for both the adult° and the newborninfant.3° Furthermore, carcass analysis reveals a lower potassium content per kilogram of lean body mass for the newborninfant than for the adult (Table I). Thesame is true for animals.2,3,12 It is notknown at what age the transition from infantile to adult composition is complete inman. For the older child and adolescent,however, the error involved is probablyrather small.

Comparisons between the potassium and

total body water methods show that somewhat larger values for fat content are obtamed by the former. °

The whole body scintillation counter isan expensive and intricate instrument, andonly a few are in existence. However, theactual procedure of measuring the adultsubject requires only a few minutes (3 to

30, depending on the instrument) and involves no discomfort to the subject.

Currently there is a great deal of interestin fat determination in living man, due primanly to the postulated relationship between obesity and disease and longevity.

* This is to be expected, since the potassium

content of the fat-free component of adipose tissueis somewhat less than that of lean tissue while thewater content is comparable for both (see secondpreceding footnote). Thus, in an obese individual,the potassium content of the total lean body massmight be somewhat less than that of a leaner subject, and so lead to an overestimation of fat content by the formula just given. On the other hand,deuterium and tritium undergo exchange with nonaqueous hydrogen, so that the total body watermethod would tend to underestimate fat content.

Unfortunately, with the exception of the use

of fat soluble indicators, all of the methodsnow available are indirect in nature anddepend for their worthwhileness on thevalidity of the underlying assumptions thatmust be made. There is no way at present ito test these assumptions other than bycomparison with carcass analysis (and theseare all too few in number and include norepresentative subject between the newborninfant and adult) or by analogy with datafrom animals. Although it is true that theindividual tissues do not differ greatly incomposition from one mammalian speciesto another, it is by no means certain thatthe relative amounts of the various tissuesare the same. This is indeed the case forskeleton; in the rat this tissue comprisesabout 7% of total body weight,b02 and inman 16%.@@

Investigators in this field are wont tocompare one method with another and touse such comparisons as a basis for drawing

conclusions as to the accuracy of one of themethods. Since no one method has as yetbeen shown to possess inherent precision,such comparison would appear fruitless. °

One other consideration has to do withthe analytic error involved in the variousmethods. For example, a determination oftotal body water involves three measurements : amount of substance injected,amount excreted, and serum concentration(a fourth is necessaryif a pre-injectionserum blank is used). All of these measurements are subject to analytic error. Theover-all error is probably of the order of 5%.This will inevitably lead (except for a subject whose fat content is 50% or greater)

* A study of the correlations of various body

measurements with fat content determined by K'°counting has recently been carried out in the author's laboratory by Dr. James Barter (unpublished).In a series of 50 adult males (20 to 55 years old)the following correlations with total fat were obtamed: body weight 0.85, skinfold thickness (av.of 6 sites) 0.73, abdominal circumference 0.90,buttocks circumference 0.87, chest circumference0.86. Over the weight range of 56-102 kg, total fat(kg) = 0.815 weight (kg) —¿�36.7, with standarderror of estimate .±5.3. Females have a higher fat

content for a given body weight.

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REPORT OF COMMITTEEON NUTRITION 489

to a larger error in estimation of fat contentthan was involved in the measurementof total body water. °

Most of the studies of fatness-leannesshave been done with adults. It is to be hopedhat some of the newer methods will be

applied to infants and children. A readilyapplicable index of this aspect of body composition would be most helpful in assessingnutritive status.

CAN BODY COMPOSITION BECHANGED BY DIET?

The question of whether body composition can be changed by diet has intriguedpediatricians for many years. Metabolicbalance studies with normal infants haveshown with monotonous regularity that theretention of nitrogen and minerals variesdirectly with intake, and calculations basedon these data showed that the greater theintake of particular substance the greaterwas its final concentration per unit weightof body. The logical conclusion was thatstorage of protein and minerals could occur,and the concept of “¿�supermmneralization―developed. General nutritional theory embraced the concept of “¿�reserve―supplies ofnutrients, and cow's milk with its greatercontent of protein and minerals wasthought to possess a definite advantage.f

It has been known for a long time thatthe calcium content of the body can bealtered by 105and recent roentgenographic observations show that the bones ofmalnourished Indian boys are less densethan those of American boys. The fat content of the body can be changed by diet.Qualitative changes in composition of bodyfat can also be produced by altering the

0 Assume body weight 60 kg, total water content

36 1; then fat = 60-36/0.72 = 10 kg, or 16.7%ofbody weight. If total water is figured at 34.2 1(5% less than 36 1), fat = 12.5 kg, or 20.8%. Thelatter value for per cent fat is 125%of the former.In general, since fat weight involves a subtractionof lean body mass from total weight, the thinnerthe person the greater will be the error, assuminga fixed error in the measurement of total bodywater.

I Cf. Fomon's critique of metabolic balancemethodology.―

type of fat fed.10°Recently the question of whether the

composition of other body tissues is subject to dietary influence (short of actualpathologic states) has been once again takenup by a number of investigators. The experiments of Wallace et al.107 with the rat,and of Filer et al.@°8with the pig, can beoffered as examples. Diets of varying protein, fat, and ash content were fed to growing animals, and the resultant compositionof the body was determined by directchemical analysis. The entire body wasanalyzed in the case of the rat, the cxsanguinated eviscerated carcass of the pig.Despite rather wide variations in diet, theseexperiments demonstrated that tissue composition generally remained rather constantwhen the values were calculated per unitfat-free tissue. Thus a unit weight (fat-free)of animal manifests a particular percentagecomposition regardless of a varying intakeof essential nutrients. The one notable cxception was calcium, which varied with theamount contained in the diet. This was truefor both the rat and pig. As Wallace et al.have put it, “¿�Thecomposition of the bodyachieves an independence from the environment.―

Widdowson et al.'°9 have recently reexamined this question. By seeing to it thatnursing rats received either a large or smallintake of milk from a very early age, theywere able to observe a number of consequences. The well-fed animals wereheavier, longer, and fatter at weaning,― andit is of great interest that these differencespersisted to a degree after weaning in theface of ad libitum feeding. In the experience of these authors this early feeding cxperience had a profound influence on bodysize and degree of fatness later in life.Moreover, these changes occurred, in contrast to the experiments cited above, on adiet of normal composition. The implications in human nutrition are obvious.

It was also found that such other pa

* The well-fed animals weighed about twice as

much and contained about four times as much fatas the poorly fed ones.

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490 BODY COMPOSITION

rameters of maturation as skeletal ossification, tooth eruption, testes size, and time ofvaginal opening were all accelerated in thewell-fed animals. Slight differences werealso found in chemical composition ofmuscle, brain, and bone; but unfortunatelynot enough data are given for these featuresto allow one to judge whether the changeswere significant. These results are in keeping with the well-known observation thatobese children show some acceleration inheight and in maturation.

The recent experiments of Heggenesset al.hbo on the rat have confirmed theseobservations in part. Overfed nursling animals grew faster, and laid down more fat,than underfed animals. However, percentage of water in the fat-free body was unchanged, as was the rate of developmentas indicated by hair appearance and eyeopening.

The feeding regimen, as well as the totalamount of food, is also important. Heggeness111 has found, for example, that weanling rats fed a high carbohydrate diet at alevel just sufficient to maintain body weightdiffer from those fed ad libitum. These differences are manifested by lack of calorigenic response to glucose feeding, by amore efficient use of diet (weight gain pergram of food consumed), and by a tendencyto store more fat. Experiments such as theseillustrate the manifold complexities of dietary factors which affect body composition.

In such experiments, the frames of reference for expressing composition must beexamined. With the exception of fat andcalcium, it has been difficult to producestriking changes in percentage compositionby altering the diet. When values are cxpressed on a per animal basis, this relativeconstancy disappears. Thus, high-proteindiets result in larger animals and, therefore,in more total accumulation of protein overa period of time than low-protein diets;high-caloric diets produce fatter animals,and the same trend is noted for some of themineral constituents. It is in this area ofinterest that the metabolic balance methodmay have some usefulness. Since the size of

the skeleton varies with diet, it is to beexpected that to a certain extent the retention of other materials that go into bonesodium, magnesium, phosphorus, and protein—will show concordant changes.

A word should be said about the phenomenon of adaptation to varying nutritional sitnations. Observations on children in technologically underdeveloped areas reveal

that these people are small in size whencompared to Western Europeans andAmericans. Thus retardation in growth ratecan be considered as an adaptation to theinadequate food supply. Newman―2 hasfound, for instance, that among adults theratio of body weight to surface area decreases as the climate becomes warmer;this is in essence an adaptation to climate.Thus the phenomenon of adaptability is

certainly not limited to lower animals, andthough it may not be as highly developedin man, it must be considered and dealtwith in evaluating studies of human nutrition.

Finally, note should be taken of recentattempts to apply some of the newer methods for the assessment of body compositionto the study of infants and children. Oslerand Pedersen113 determined total bodywater in a series of newborn infants born todiabetic mothers, with the interesting resultthat these infants have a subnormal watercontent, and thus probably an increasedamount of fat. Smith114 made a study oftotal body water in malnourished infants.Composition underwent marked changesduring recovery, including periods whengain in body weight was poor. ParIzková63has measured body density in a series ofnormal and obese children; density was

markedly reduced in the latter group.

CONCLUDING REMARKS

At attempt has been made in this reviewto present the various methods for estimation of body composition which are available to the modern investigator. Not all ofthem are well suited to the study of infantsand children, and some require an intricatetechnology. Generally, they do not comrn

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REPORT OF COMMITTEE ON NUTRITION 491

13. Dickerson, J. W. T., and Widdowson, E. M.:Chemical changes in muscle during development. Biochem. J. 74:247, 1960.

14. Metcoff, J. : In Physiology of Prematurity,edited by J. Lanman, 4th Macy Conference,

1960.15. Metcoff, J., et al.: Relations of intracellular

ions to metabolic sequences in muscle inKwashiorkor. PEDIATRICS,26:960, 1960.

16. Waelsch, H., ed, Biochemistry of the Dcveloping Central Nervous System, NewYork, Academic Press, 1955.

17. Yieng, M. J., Barrows, C. H., Jr., and Shock,N. W. : Age changes in the chemical cornposition of muscle and liver in the rat.J. Geront., 14:400, 1959.

18. Dickerson, J. W. T., McCance, R. A., andWiddowson, E. M. : Severe malnutrition ingrowing and adult animals. Brit. J. Nutr.,

14:331, 457, 1960.

19. Forbes, G. B. : Studies on sodium in bone.

J. Pediat., 56:180, 1960.20. Hammett, F. S. : A biochemical study of bone

growth. J. Biol. Chem., 64:409, 685, 693,1925.

21. Breibart, S., et al.: Relation of age to radiomagnesium exchange in bone. Proc. Soc.

Exp. Biol. Med., 105:361, 1960.22. Friis-Hansen, B. J., et al.: Total body water

in children. PEDIAmIcs, 7:321, 1951.23. Reid, J. T., Balch, C. C., and Glascock, R. F.:

Use of tritium, of antipyrine and of N-acetyl-4-amino-antipyrine in the measure

ment of body water in living rabbits. Brit.J. Nutr., 12:43, 1958.

24. Cheek, D. B., and West, C. D. : An appraisalof methods of tissue chloride analysis: The

total carcass chloride, exchangeable chloride, potassium and water of the rat. J.Clin. Invest., 34: 1744, 1955.

25. Edelman, I. S., et al: Further observationson total body water: I. Normal valuesthroughout the life span. Surg. Gynec.Obst.,95:1, 1952.

26. Allen, T. H., Anderson, E. C., and Langham,W. H. : Total body potassium and grossbody composition. J. Geront, 15:348, 1960.

27. Talso, P. J., et al.: Exchangeable potassiumas a parameter of body composition. Metabolism, 9:456, 1960.

28. Rundo, J., and Sagild, U. : Total and “¿�cxchangeable― potassium in humans. Nature,

175:774, 1955.29. Forbes, G. B., and Perley, A. M. : Estimation

of total body sodium by isotopic dilution.J. Clin. Invest., 30:558, 566, 1951.

30. Christian, J. R., and Talso, P.J. : Exchangeablepotassium in normal full-term newborn infants. Psnwrmcs, 23:63, 1959.

31. Christian, J. R., et al.: Total body water and

mand a high degree of precision, a statement which is all too true (though only recently admitted) for the time-honored metabolic balance technique. The very slowgrowth rate of man makes for great difficulty in applying seriatim any technique for

estimating the composition of normalgrowth over short intervals of time. Nonetileless, assessment of gross body composi

tion is an important tool for nutritionalresearch and for the study of populationgroups, and is in fact prerequisite to theunderstanding of some modern nutritionalproblems. It is to be hoped that pediatricinvestigators will make fuller use of themethods now at hand, and even partake inthe development of newer methods yet tocome.

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104. Williams, D., et al: Influence of mineral intake on bone density in humans and inrats. J. Nutr., 61 :489, 1957.

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107. Wallace, W. M., Weil, W. B., and Taylor, A.:

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72. Tanner, J. M. : i'@Ieasurement of body fat inman. Proc. Nutr. Soc., 18: 148, 1959.

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76. Lim, T. P. K., and Luft, U. C. : Body density,fat, and fat-free weight. Amer. J. Med.,

30:825, 1961.

77. Talbot, N. B. : Measurement of obesity by thecreatinine coefficient. Amer. J. Dis. Child.,55:42, 1938.

78. Clark, L. C., Jr., et al: Excretion of creatineand creatinine by children. Amer. J. Dis.Child., 81:774, 1951.

79. Stearns, G., et a!.: Protein requirement ofchildren from one to ten years of age. Ann.N.Y. Acad. Sci., 69:857, 1958.

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Acknowledgment

I should like to acknowledge the generous cooperation of Dr. E. M. Widdowson in making available to me the detailed results of her studies onbody composition of man and various mammals,and that of Dr. W. H. Langham in sending medetailed data on K―measurements.

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1962;29;477Pediatrics Gilbert B. Forbes

a Note on the Effect of Diet on Body CompositionMETHODS FOR DETERMINING COMPOSITION OF THE HUMAN BODY: With

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