Differences in skeletal muscle and bone mineral mass between black and white females and their relevance to estimates of body composition

8 Am iC/in Nuir l992;55:8- 13. Printed in USA. © 1992 American Society for Clinical Nutrition

Differences in skeletal muscle and bone mineral massbetween black and white females and their relevanceto estimates of body composition13

Oscar Ortiz, Mary Russell, Tracey L Daley, Richard N Baumgartner, Masako Waki,Steven Lichiman, Jack Wang, Richard N Pierson, Jr, and Steven B Heymsfield

ABSTRACI’ This study tested the hypothesis that black fe-

males have an increase in skeletal muscle and bone mineral

mass compared with white females matched for age (±5 y),

weight (±2 kg), height (±3 cm), and menstrual status. Conven-

tional [underwater weighing, whole body ‘�#{176}Kcounting (WBC),

3H20 dilution] and newly developed (dual-photon absorptiom-

etry) techniques were used to provide ethnicity-independent es-

timates of body composition in 28 pairs of matched subjects.

Black females had greater appendicular skeletal muscle (P

< 0.001), bone mineral (P < 0.001), and total body potassium

(TBK) (P = 0.05) compared with white females. Two classic

coefficients used in body composition research [density of fat-

free mass (FFM) for underwater weighing and TBK/FFM for

WBC] differed significantly (P < 0.05) between black and white

females; currently applied coefficients underestimated fat in black

females. This study confirms that black and white females differ

in body composition and that errors in fat estimates occur when

ethnicity is not accounted for in body composition mod-

els. AmiClinNutr l992;55:8-13.

KEY WORDS Body composition, ethnicity, obesity

Introduction

Obesity is a major health problem in the United States (1);

its prevalence varies between ethnic groups. Overall, black fe-

males between the ages of 20 and 60 y have the highest rates of

obesity and its associated complications, such as diabetes and

high blood pressure (2).

With increasing attention focusing on the relation between

ethnicity and obesity, an important concern is the accuracy of

quantifying body fat and other tissue compartments. Although

there are many body-composition techniques (3), most depend

on the assumption that ethnicity is an insignificant contributor

to the compartmental determinants ofbody weight. For example,

the widely applied body mass index (BMI; wt/ht2) is used to

classify subjects of similar age and gender, independent of

their ethnic status, into categories of equivalent body composi-

tion (4).

Despite the assumption that body composition is independent

of ethnic status, there is growing evidence that black females in

particular have a relatively larger skeletal muscle and bone min-

eral mass than do white females. Stimulated by the low osteo-

porosis fracture rate observed in black females, Cohn et al (5)

compared total body potassium (TBK) and calcium in black

females with matched white female control subjects. Both ele-

ments were increased by �-5-l0% in the black females, sug-

gesting larger skeletal muscle and bone mineral mass as com-

pared with the white female control group. Recent studies using

regional dual-photon techniques amply confirmed an increase

in bone mineral density in black females (6, 7).

If skeletal muscle and bone mineral masses differ between

black and white females, then many, if not most, body-com-

position techniques would fail to account for these ethnic dif-

ferences in the components ofbody weight and would therefore

provide inaccurate estimates of fat and other tissue compart-

ments (8- 10). Prevalence estimates of overweight and obesity

would be affected also.

Until recently investigators were limited in their capabilities

for evaluating several major body compartments, such as bone

mineral, in vivo. The introduction over the last several years of

dual-photon-absorptiometry (DPA) systems for evaluating

whole-body bone mineral mass and soft tissue composition (10-

1 2) now makes it feasible to examine the associations between

ethnicity and body composition.

The specific aim of this study was to test the hypothesis that

black and white females matched for age, weight, height, and

menstrual status differ significantly in the proportions of body

weight contributed by skeletal muscle mass and bone mineral

mass. Support for this hypothesis would imply that the two

widely used research methods of evaluating body composition,

underwater weighing (1 3) and whole-body ‘�#{176}Kcounting (14),

will be inaccurate when the currently used models are applied

to black females. A secondary aim of the study was to establish

the validity of these two methods as presently applied in black

females.

I From the Department of Medicine, Obesity Research Center, St

Luke’s-Roosevelt Hospital, Columbia University College of Physicians

and Surgeons, New York, and the Department of Pathology, Universityof New Mexico School of Medicine, Albuquerque, NM.

2 Supported by NIH grant PO1-DK428 18.3 Address reprint requests to SB Heymsfield, Weight Control Unit,

4 1 1 West 1 14th Street, New York, NY 10025.

Received January 8, 1991.Accepted for publication June 5, 1991.

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ETHNICITY AND BODY COMPOSITION 9

The between-day CVs for bone-mineral and total appendicular

Methods

Subjects

Black females aged 20-70 y were recruited in several ways.

Some were hospital employees and some were recruited through

newspaper advertisements and via leaflets circulated in the local

community. Subjects enrolled in the study met four criteria:

absence of medical illness as substantiated by medical history

and a physical examination, a BMI < 30 (in kg/m2), absence of

atypical diet history, and daily physical activities that included

full ambulation and recreational exercise. Each black female

was then matched to a white female control subject, recruited

similarly, by age (±5 y), weight (±2 kg), height (±3 cm), and

menstrual status. The white subjects met similar health, diet,

and physical-activity criteria as were established for the black

subjects. The investigation was approved by the Institutional

Review Board ofSt Luke’s-Roosevelt Hospital Center and each

subject signed an informed-consent form before the study began.

Protocol

On completion ofthe screening evaluation, subjects underwent

body-composition studies that included anthropometry, DPA,

3H20 dilution, underwater weighing, and whole-body “#{176}K

counting. The results ofthese procedures were then used to cal-

culate compartmental masses and other relevant body-compo-

sition indices.

Experimental procedures

Anthropometry. Body weight and height were measured to

within 0.01 kg and 0. 10 cm by using an electronic scale (Weight-

Tronix, Scale Electronics Development, New York) and stadi-

ometer (Holtain Limited, Crosswell, Wales, UK), respectively.

Waist and hip circumferences were measured at the costal margin

and at the maximum horizontal girth between waist and thigh

by using a steel measuring tape, as defined in the Airlie Confer-

ence proceedings (15).

Dual-photon absorptiometry. A whole-body DPA scanner(DP-

4, Lunar Radiation, Madison, WI) was used to quantify total-

body and regional bone-mineral and appendicular skeletal mus-

cle mass as previously described (1 3, 16). Each patient scan,

requiring ‘-50 mm, was followed by studies ofseven frozen beef

phantoms of known fat content. On the basis of the phantom

calibrations, the ratio of soft-tissue attenuations (R5�) at the

scanner’s two energy levels (7 and 16 fI) was used to partition

soft tissue into fat and lean components.

On analysis of the patient’s scan, the DPA instrument’s soft-

ware allowed separation of the body into six regions, including

upper and lower appendages ( 16). Bone mineral mass and RST

were then calculated by system software for the whole body and

for the upper and lower appendages. The appendicular soft tissue

was then further divided into fat and fat-free components by

using the measured R�- and the soft-tissue phantom calibration.

We assumed that the fat-free and bone-mineral-free mass of the

appendages represented skeletal muscle plus a small and rela-

tively constant skin mass. Details of the calculations involved

are presented elsewhere ( 16). We previously demonstrated good

correlations between skeletal muscle mass by using this method

compared with other noninvasive techniques ofestimating skel-

etal muscle (16). Appendicular skeletal muscle represents about

two-thirds to three-fourths of total-body-skeletal-muscle mass.

skeletal muscle, as measured by DPA, are 1 .0% and 3.0%, re-

spectively.

The long-bone lengths in the upper (neck of the humerus to

styloid process of ulna) and lower (neck of the femur to medial

malleolus of the tibia) extremities were measured in the DPA

scan. The actual length of the extremity long bones was then

calculated by using the ratio of total body length in the scan to

actual height as an internal standard.

3H20 dilution. Subjects received 0.19 Bq 3H2O, which was

followed by a 3-h blood sample (17). The 3H2O-dilution volume

was calculated after correction for urinary isotope losses. The

CV for this procedure is 1 .5%. Total-body-water volume was

estimated as the 3H2O dilution space X 0.95, based on correction

for nonaqueous hydrogen exchange. Aqueous mass was calcu-

lated as the product oftotal-body-water volume and water density

at 37 #{176}C(0.994 g/cm3).

Underwater weighing. Body density was measured by using

water submersion in a previously described four-point platform

scale system (1 8). Body density was calculated after adjustment

for water temperature and for residual lung volume, the latter

established after underwater weighing by using the system de-

scribed by Wilmore (19). The CV for body density derived by

underwater weighing is 0.4% at our Center.

Whole-body 40K counting. TBK was evaluated in a 4-ir whole-

body counter (20, 2 1). Adjustments in the raw counts were made

for body size based on a previously reported 42K calibration

study (2 1). The CV for the 9-mm counting procedure is 3%.

Body-composition calculations

The DPA study provided estimates oftotal-body and regional

bone mineral mass and bone density and appendicular-skeletal-

muscle mass. Body weight was also compartmentalized into

mineral, water, protein, and fat by using a method based on

measured bone mineral (DPA), 3H2O dilution volume, and body

density (underwater weighing) (20). Briefly, bone mineral (mea-

sured by DPA) is first adjusted upward to total body mineral by

using data detailed in previous cadaver studies (10). Body density

is then corrected for mineral and water densities (3.042 and

0.994 g/cm3, respectively), the remainder representing the con-

tributions of protein and fat (1 .340 and 0.900 g/cm3, respec-

tively). Note that these compartmental densities represent phys-

ical properties ofthe chemical compounds involved and therefore

should not be confused with the density value of bone that is

provided by DPA. The combined mass ofprotein and fat is then

calculated by subtracting mineral and aqueous mass from body

weight. Lastly, fat mass is estimated given the mass and density

ofthe protein plus fat mixture (Eq 1, Table 1). In sum, estimatedbone mineral, 3H2O-dilution volume, and body density are used

to separate body weight into four components: mineral, protein,water, and fat.

The importance of this approach in estimating fat is that no

assumptions are made that could potentially be confounded by

ethnic status, age, or gender. Previous studies show excellent

agreement between results from using this four-compartment

model and those derived by using neutron-activation method-

ology (20). The CV for fat mass estimated by this approach is

3.0%, and fat-free mass (FFM) is considered to be the sum of

protein, water, and mineral.

Two conventional reference methods of estimating body fat

are underwater weighing and whole-body �‘#{176}Kcounting (14). The

primary assumption ofthe underwater-weighing method is that

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10 ORTIZ ET AL

5 1 ± SD (range); n = 28.

t In kg/m2.

TABLE 1Equations used to estimate fat and density of fat-free body mass5

Number(ref) Equation

1 (20) Fat(kg) = [BW-(A + M)][�!�-�_ 205]DP+F

2 (3) Fat (kg) = [BW] [� - 4.50]

3(10) d���1(g/cm3) = [(1.0063 X fA) + (0.7463 X fP)

+ (0.3287 fM)]’

S A, aqueous mass (in kg); BW, body weight (in kg); Db, body density(in g/cm3); dFFM, density of FFM (in g/cm3); DP+F, density of proteinplus fat (in g/cm3); f, fraction; M, total body mineral (in kg); and P,protein (in kg).

the densities of fat and FFM are 0.900 and 1 . 100 g/cm3, re-

spectively. According to this method, total body fat is calculated

as presented in equation 2 (Table 1). A relative increase in the

bone mineral (whose density is 3.042 g/cm3) content of FFM

could increase the density of FFM in black females, thereby

causing errors in fat estimates. Similarly, a relative decrease in

the hydration ofthe FFM could increase its density. We explored

these possibilities by directly calculating the density of FFM

(dFFM) based on the four-compartment estimates as shown in

equation 3 (Table 1).

The primary assumption of the whole-body-’#{176}K-counting

method is that the potassium concentration ofFFM on the basis

of an individual’s age and gender is known and constant (14,

17). At our center the value of 59.8 mmol/kg was established

for healthy white females (n = 30, age 4 1 .9 ± 4.7 y) aged 35-

49 y and is the presently used appropriate constant for estimating

fat in the TBK model. According to this method, FFM (in kg)

is first calculated as TBK (in mmol)/59.8, and fat (in kg) is then

equal to body weight - FFM.

Statistical analysis

Some of the subjects were unable to complete all of the pro-

cedures, eg, underwater weighing because offear of submersion,

or whole-body counting because of claustrophobia. The total

number of paired subjects therefore varies for each body-com-

position comparison between black and white females. Between-

group differences for each body-composition estimate were

evaluated by two-tailed paired t tests. Results are presented as

group means ± SDs.

Results

The baseline information for subject evaluation is presented

in Table 2. A total of 28 black females and respective white

female control subjects met the four study-entry criteria. There

were no significant differences between the groups in age, height,

weight, and BMI. The study groups were, on average, middle-

aged (44.2 and 43.6 y) and the mean BMIs for both groups (23.9

and 23.6) approximated the 50th percentile for nationally rep-

resentative samples ofblack and white women (22). There were

no significant differences between the groups in body-fat distri-

bution as indicated by the waist-to-hip ratio in black (0.81 ± 0.05)

vs white (0.80 ± 0.04) females.

The results ofbody-composition studies are presented in Table

3. Both TBK and bone mineral were significantly increased by

8.0% and 13.8% (P = 0.05 and P < 0.001) in black females

relative to their matched white counterparts. Total bone density

in the black females was 1. 18 ± 0. 14 g/cm2, which was signifi-

cantly (n = 28 pairs; P < 0.001) higher than the bone density

observed in white females (1.09 ± 0.09 g/cm2).

Results for appendicular skeletal muscle and bone mineral

are presented in Table 4. Black females had greater skeletal mus-

cle and bone mineral in the upper (both P < 0.001), lower (both

P < 0.01), and combined extremities (+14.6%, +16.2%; both P

< 0.001) than did white females. Both the upper- and lower-

extremity bone lengths (n = 28 pairs) were significantly (P < 0.05

and P < 0.01, respectively) longer in the black females (53.8

± 7.5 and 80.3 ± 10.4 cm) by -2 cm than in the white females

(52.7 ± 4.2 and 78.1 ± 6.2 cm).

The total appendicular-skeletal-muscle mass was combined

with total-body bone mineral to provide an estimate of mus-

culoskeletal mass (n = 28 pairs). Black females had 20.6 ± 3.6

kg of musculoskeletal mass, which was 14.7% higher than that

observed in white females (18.0 ± 2. 1 kg, P < 0.004). Overall,

musculoskeletal mass represented 33 ± 5% and 29 ± 3% of body

weight in black and white females (P < 0.002), respectively.

The results of two-compartment, body-composition-model

coefficients-dFFM and K/FFM-in black and white females are

presented in Table 5. Both dFFM and K/FFM were significantly

(P < 0.05) higher in black than in white females. The hydration

of FFM (ie, total body water/FFM) was similar between black

and white subjects (n = 19; 0.734 ± 0.041 vs 0.747 ± 0.037 (NS).

The ethnically distinct coefficient for density and potassium

content of FFM (ie, dFFM and K/FFM) implies that systematic

errors are made in the estimate of percent body fat when tra-

ditional underwater-weighing and whole-body-”#{176}K (dFFM = 1.100

g/cm3 and TBK/FFM = 59.8 mmol/kg) models are used in black

females. This subtle measurement bias is demonstrated in Table

6, which presents percent body fat for black and white females

derived by traditional underwater-weighing and whole-body-�#{176}K

methods and by our assumption-independent four-compartment

model in the 17 pairs ofwomen in whom all ofthe measurements

were available. Although in white females the underwater-

weighing and whole-body-�#{176}K methods provided larger results

for percentage fat than did the four-compartment model, they

underestimate fat in black females. Had these two-compartment

methods been used to compare black and white females in the

TABLE 2Baseline r esults for blac k and matched-w hite female grou ps5

Body massGroup Age

y

Weight

kg

Height

m

indext

Black 44.2 ± 15.2

(24-79)

62.3 ± 5.8(50.3-78.5)

1.61 ± 5.8( 1 .52- 1 .73)

23.9 ± 2.5

(20.0-29.3)

White 43.6 ± 15.3

(24-78)

62.0 ± 6.6

(50.8-76.7)

1.62 ± 5.7

( 1.50-1 .72)23.6 ± 2.2

( I 9.6-28.2)

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ETHNICITY AND BODY COMPOSITION 11

5 1 ± SD (range); n = 28 matched pairs.

t� Significantly different from blacks: tP < 0.001, jP < 0.01.

TABLE 3Body compo sition in black and m atched-white female groups5

TBW(n = 19)

db(n = 21)

TBK(n = 25)

Bone mineral(n = 28)

Fat(n = 19)

FFM(n = 19)

L g/cm3 mmo/ kg % kg

Black

White

33.1 ± 5.1

(27.0-44.7)33.0 ± 4.0

(26.5-41 .2)

1.039 ± 0.016

( I .01 2-1 .068)1.032 ± 0.016

( 1 .010-1 .075)

2703 ± 508

( I 867-356 1)

2502 ± 403t( 1892-3302)

2.64 ± 0.49

( 1.62-3.67)2.32 ± 0.33�

( 1.53-2.87)

27.9 ± 7.3

( 14.3-40.0)

28.9 ± 5.9

(5.9-40.0)

45.1 ± 6.3

(36.4-59.5)44.2 ± 5.1

(36.0-54.7)

5 1 ± SD (range). TBW, total body water.

if Significantly different from blacks: tP = 0.05, fP < 0.001.

present study, percent fat would have been borderline or signif-

icantly lower in black than in white females (P < 0. 1 for un-

derwater weighing and < 0.01 for ‘�#{176}K).Because the measurement

bias in fat estimates in the black females for the underwater-

weighing (�%fat = - 1.6% vs four-compartment) and whole-

body-’�#{176}Kmethods (�%fat = -3.9%) is relatively small, a larger

study population would be required to detect the expected sig-

nificant within-group differences among the three methods.

Discussion

The results of this study confirm the hypothesis that black

and white females of equivalent age, weight, height, and men-

strual status differ significantly in body composition. Specifically,

the black females had 10-15% more appendicular skeletal muscle

and total bone mineral mass than their white counterparts. In

contrast, neither total FFM nor total body water were signifi-

cantly different between the two ethnic groups (Table 3). The

result was that both dFFM and K/FFM were increased significantly

in black vs white females.

The average potassium concentration oftotal lean tissue was

increased in black females because oftheir larger appendicular-

skeletal-muscle mass and the fact that skeletal muscle has a rel-

atively high fraction of its weight as potassium-rich cell mass

(92 mmol/kg fat-free weight) compared with the remaining vis-

ceral tissue (64 mmol/kg fat-free weight)(23). Although our DPA

method allowed only for a direct estimate ofappendicular skeletal

muscle, the significantly higher K/FFM in black females implies

TABLE 4

that whole-body skeletal muscle is also greater in black females

than in white females (24).

The density oftotal FFM was higher in black females because

the fraction oflean tissue represented by high-density bone mm-

eral was increased above that observed in white females. Thus,

two-compartment body-composition methods based on under-

water weighing and whole-body �#{176}Kcounting clearly need ad-

justments when applied to black females. We emphasize that

the magnitude of these corrections appears small as suggested

by the results presented in Tables 5 and 6. Nevertheless, a critical

analysis ofthe relation between ethnicity and body composition

requires models and methodologies that go beyond the under-

water-weighing and whole-body-”#{176}K counting methods as they

are now applied. This is particularly the case when examining

body composition across ethnic groups, as was the case in the

present study.

Although underwater-weighing and whole-body counting

methods are largely research techniques, they are widely used

to calibrate most clinical and epidemiologic approaches to an-

alyzing body composition (25). For example, anthropometric

prediction of body fat is accomplished by developing multiple-

regression equations based on skinfold thicknesses at several an-

atomic locations by using underwater weighing as the reference

method ofquantifying fat (26). Reconsideration should therefore

be given to the choice of criterion methods when developing

body-composition prediction equations in ethnically diverse

populations.

Note that present body-composition models may also need

further refinement for use in white females, a process made pos-

Values for appendicular skeletal muscle (SM) and regional bone mineral (bone) for black and white females matched for age, height, weight, and

menstrual status5

Upper extremities Lowe r extremities Total appendicular

SM Bone SM Bone SM Bone

kg

Black

White

6.1 ± 1.3

(4.0-9.4)4.8 ± l.2t

(2.6-8.3)

0.31 ± 0.06

(0. 19-0.42)

0.25 ± 0.04t

(0. 16-0.32)

1 1.9 ± 2.1

(8. 1- 17.0)10.9 ± l.6j

(8.5- 14.6)

0.91 ± 0.19

(0.50- 1.3 1)0.80 ± 0.l3�

(0.52- 1 .0 1)

18.0 ± 3.0

( I 2.7-25.0)

15.7 ± 2.2t

( 1 2.0- 19.4)

1.22 ± 0.25

(0.69-1.76)1.05 ± 0.17t

(0.68-1.32)

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S � � SD (range).

tt Significantly different from blacks: tP < 0.02, tP < 0.03.

12

sible by advances in body-composition methodology (27). Mod-

els based on neutron-activation techniques (27-29) are capable

of providing investigators with an accurate and precise quanti-

fication of multiple body compartments in vivo in a manner

independent of potentially ethnically biased methods. This ap-

proach will ultimately replace the previous criterion cadaver

technique, which has always suffered from a paucity ofdata and

a lack of ethnic specificity.

Although the mechanisms leading to an increased musculo-

skeletal mass in black females remains unknown, present cvi-

dence suggests that the process begins in utero (30) and involves

metabolic determinants ofbone formation (3 1, 32). Bone length

and weight are greater in black than in white fetuses, and this

ethnic difference persists throughout life (33). Blacks have a

higher density of all bones examined, including weight-bearing

and nonweight-bearing areas ofthe skeleton (33). The divergence

between bone mineral content and density remains after ad-

justment for BMI, level ofphysical activity, and dietary calcium

intake (34). A higher bone density and greater appendicular bone

length was also observed in the adult black females evaluated

in the present study.

Bell et al (3 1) observed greater serum immunoreactive para-

thyroid hormone and 1,25-dihydroxyvitamin D concentrations

in blacks than in whites who were maintained on constant diets.

Weinstein and Bell (32), using histomorphometric measurement

techniques, detected a diminished rate of bone formation in

blacks compared with whites. This reduced rate ofbone remod-

cling, according to the authors, may contribute to the preser-

vation of bone mass and reduced rate of osteoporosis observed

in older black females. Serum calcitonin, a bone trophic hor-

mone, is greater in Gambian and West Indian blacks than in

comparable white control groups (35, 36).

Although direct evidence for the mechanisms of increased

skeletal muscle mass is lacking, muscle and bone mass are usually

highly correlated (37). Hence, skeletal muscle mass in black fe-males may be greater than in white females because ofthe afore-

mentioned primary mechanisms influencing bone length and

weight. Another alternative is that increased physical activity in

black females stimulates concurrent development ofboth skeletal

muscle and bone mineral (33). Although this possibility cannot

be excluded, our review ofphysical-activity histories (time spent

in 10 activities/wk, mo, and y) demonstrated no overall differ-

ences in exercise level or pattern between the two groups. As in

earlier studies, we also observed increased bone mineral (and

skeletal muscle) in the nonweight-bearing upper extremities (33).

TABLE 5

Density ofand potassium concentration in FFM in the black and

matched-white female groups

dFFM

(n=19)K/FFM

(n=19)

g/cm3 mmol/kg

Black 1.106 ± 0.013(1.091-1.146)

63.1 ± 8.4(45.1-77.4)

White 1.097 ± 0.009t

(1.070-1.1 14)

56.6 ± 7.4�

(42.7-66.4)

ORTIZ ET AL

TABLE 6Percent total body fat in black and white females (n = 17 pairs)estimated by using traditional and ethnically independent models5

Method Black White

Underwater weighing 26.5 ± 7.8 30.2 ± 7.4t

Whole-body-�#{176}K counting 24.2 ± 1 1.5 32.8 ± 12.2f

Four compartment 28.1 ± 7.6 29.3 ± 7.7

S � � SD.

if Significantly different from blacks: tP < 0. 1, �P < 0.01.

Although the mechanisms ofobserved ethnic differences in body

composition remain unresolved, presently available information

suggests that inherited rather than environmental influences are

the main factors involved.

In conclusion, this investigation demonstrates that matched

black and white females differ significantly in the proportion of

body weight as skeletal muscle and bone mineral mass. As a

result, two widely used body-composition methods that were

derived and validated in whites underestimate body fat in black

females. These results have important implications for the study

of human body composition and the interpretation of body

weight in research laboratories, clinical settings, and field

surveys. B

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