1 Department of Medicine, Obesity Research Center, St. Luke's-Roosevelt Hospital, Columbia University, New York, New York 10025; and 2 Departments of Medicine and Chemistry, University of Vermont, Burlington, Vermont 05405
![]() |
ABSTRACT |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
We sought to determine if
decrements in the mass of fat-free body mass (FFM) and other lean
tissue compartments, and related changes in protein metabolism, are
appropriate for weight loss in obese older women. Subjects were 14 healthy weight-stable obese (BMI 30 kg/m2) postmenopausal
women >55 yr who participated in a 16-wk, 1,200 kcal/day nutritionally
complete diet. Measures at baseline and 16 wk included FFM and
appendicular lean soft tissue (LST) by dual-energy X-ray
absorptiometry; body cell mass (BCM) by 40K whole body
counting; total body water (TBW) by tritium dilution; skeletal muscle
(SM) by whole body MRI; and fasting whole body protein metabolism
through L-[1-13C]leucine kinetics. Mean
weight loss (±SD) was 9.6 ± 3.0 kg (P < 0.0001)
or 10.7% of initial body weight. FFM decreased by 2.1 ± 2.6 kg
(P = 0.006), or 19.5% of weight loss, and did not
differ from that reported (2.3 ± 0.7 kg). Relative losses of SM,
LST, TBW, and BCM were consistent with reductions in body weight and FFM. Changes in [13C]leucine flux, oxidation, and
synthesis rates were not significant. Follow-up of 11 subjects at
23.7 ± 5.7 mo showed body weight and fat mass to be below
baseline values; FFM was nonsignificantly reduced. Weight loss was
accompanied by body composition and protein kinetic changes that appear
appropriate for the magnitude of body mass change, thus failing to
support the concern that diet-induced weight loss in obese
postmenopausal women produces disproportionate LST losses.
obesity treatment; skeletal muscle mass
![]() |
INTRODUCTION |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
OBESITY IS AN INCREASING PROBLEM among Americans (20), particularly elderly women (20). Although weight loss is typically recommended by clinicians for younger obese subjects (17), some concerns exist regarding the prescription of weight loss treatments for older individuals.
The first concern is that older subjects may already have, or are at increased risk of developing, the chronic diseases associated with old age (8). Accordingly, most practitioners assume that higher body weights with ample endogenous nutrient stores at the outset of a chronic illness afford some long-term protection during potential periods of undernutrition.
A second prevailing concern with weight loss treatment of the elderly is that it remains unresolved whether excessive adiposity poses health risks in older individuals as it does in younger adults (3). Nevertheless, many older individuals enroll in weight loss programs or purchase weight loss products in the hope of restoring body weight to levels maintained earlier in life.
A third concern, and the focus of the present investigation, is based on the observation that senescence in humans is associated with loss of lean tissues, particularly fat-free body mass (FFM) and its main component, skeletal muscle (SM) (10, 12, 39). Elderly obese subjects may therefore have a reduced lean tissue mass at the commencement of a weight loss program. A concern is that weight loss treatment, unless accompanied by vigorous physical activity, may produce excessive lean tissue losses in the elderly, including FFM, SM, body cell mass (BCM), and other functionally important components such as bone mineral (33). Whether or not lean tissue losses with dieting are actually disproportionate in the elderly relative to those observed in younger subjects remains untested, although anabolic potential and protein metabolic processes in the elderly differ from those of younger subjects.
The aim of this prospective study was to test the hypothesis that obese postmenopausal women would demonstrate a disproportionate loss in FFM with weight loss produced by a hypocaloric diet. To test this hypothesis, we compared the effects of dieting on FFM in obese postmenopausal women in the present study with FFM changes reported after weight loss in young obese women. A secondary aim was to gain further insight into the disproportionate reductions in FFM by measuring whole body protein synthesis and breakdown and other lean tissue components before and after the period of weight loss.
![]() |
METHODS |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Experimental Design
The changes in body composition and protein metabolism observed after a 16-wk weight loss treatment program were first examined. Body weight and body composition evaluations were then repeated after a 1- to 2-yr follow-up period.The hypothesis was tested by comparing changes in FFM observed in the postmenopausal women after the 16-wk weight loss phase and subsequent follow-up phase with those of young obese women reported in earlier studies.
Subjects
Obese postmenopausal women.
Subjects were obese postmenopausal women with a body mass index (BMI)
of 30BMI
40 kg/m2, and without a history of
cardiovascular disease, diabetes mellitus, or high blood pressure.
Inclusion criteria required that subjects be
5 yr since menopause,
ambulatory, nonexercising, and nonsmoking and have maintained current
body weight ±3 kg in the preceding 6 mo. Subjects on estrogen
replacement therapy or those who were taking other medications that
could potentially influence body composition or protein metabolism were
excluded from the study. Recruitment occurred through advertisements in
newspapers and flyers posted in the local community.
Reference group.
The hypothesis was tested by comparing the observed reduction in FFM
relative to body weight (i.e., FFM/
BW) with that published in a
literature compilation for young dieting obese women (1) at two time points, 16 wk and 2-yr follow-up.
Experimental Procedures
During a screening visit to the Center, each experimental subject completed a medical examination that included blood tests, blood pressure, electrocardiogram, and a gallbladder ultrasound after an overnight fast. Only subjects without diagnosed medical conditions were enrolled in the weight loss study. Specifically, subjects with diabetes (fasting blood glucose >140 mg/dl) or high blood pressure (>140 mmHg systolic or >90 mmHg diastolic) were excluded from the study. The investigation was approved by the Institutional Review Board of St. Luke's-Roosevelt Hospital, and all subjects gave written consent to participate.Weight Control Program
Protocol.
Enrolled subjects participated in 2 days of testing, at baseline
and after the 16-wk weight loss phase. Subjects reported on the morning
of day 1 in a fasted state (8 h) to the Human Body
Composition Laboratory, where body composition studies were carried out
in the morning and afternoon. Blood samples were taken and sent to a
commercial laboratory (Quest Diagnostics, Teterboro, NJ) for analysis
of serum electrolytes, liver function tests, lipids, and glucose.
Diet. During the 2 days of baseline tests, subjects consumed a liquid diet (Sustacal: 15% protein, 45% carbohydrate, 40% fat) equivalent in energy to 1.25 × resting energy expenditure (~1,800 kcal and 0.8 g protein/kg per day). During the 16-wk weight loss phase, subjects were counseled to eat a 1,200 kcal and ~0.7 g protein/kg per day diet. Prepackaged breakfasts, lunches, dinners, snacks, and multivitamins were provided to the subjects, who supplemented their diet with fresh fruits and vegetables. The recommended diet had 15-20, 50-60, and 25-30% of total calories as protein, carbohydrates, and fat, respectively.
Body Composition Analysis
The evaluated body composition compartments spanned three body composition levels, molecular, cellular, and tissue system (38). FFM and four of its major components, appendicular lean soft tissue (LST, a measure of SM) mass, total body water (TBW), BCM, and bone mineral mass were evaluated in each subject before and after the 16-wk weight loss phase. Total body SM mass was also evaluated in a subgroup of subjects.Observed LST (i.e., SM, BCM, and TBW) changes were qualitatively examined for appropriateness relative to changes in FFM. FFM and closely related adipose tissue-free mass are approximately one-half of SM, one-third of BCM, and three-fourths of water (35). These explorations were aimed at searching for extreme deviations, such as a disproportionately large weight change accounted for largely by either water (i.e., fluid) or SM.
TBW was quantified by tritium dilution (28), and FFM,
appendicular LST mass, and bone mineral mass were quantified by
dual-energy X-ray absorptiometry (DEXA) (16). BCM
was estimated using total body potassium (TBK) as derived by counting
the natural -ray decay of 40K in a whole body counter
(29). Total body SM mass was evaluated by whole body
multislice magnetic resonance imaging (MRI) (15, 32). Subjects on whom MRI studies were performed were
selected on the basis of scanner availability at baseline, and repeat
studies were performed at the 16-wk evaluation.
The labeled leucine study was designed to evaluate protein dynamics (22) in relation to changes in protein-containing FFM.
Lipid compartment measurements included total body fat by DEXA in all subjects and total body and visceral adipose tissue by MRI (15, 32) in the same subgroup of subjects that completed SM studies.
The weight-maintenance body composition reevaluation included evaluation of selected lean components, including FFM, appendicular LST, and BCM.
Body weight and height were measured to the nearest 0.1 kg and 0.5 cm with a digital scale (Weight Tronix; New York, NY) and stadiometer (Holtain; Crosswell, Wales), respectively. Waist and hip circumferences were measured while the subjects were wearing only their undergarments and standing with their heels together. Minimum waist circumference was measured between the lower rib margin and iliac crest. Maximum hip circumference was measured below the iliac crest, with the subject viewed from the front.
DEXA. A slow-mode DEXA scan (DPX, software version 3.6; Lunar Radiation, Madison, WI) was used in all studies before and after weight loss. The DEXA system provided an estimate of total body fat, with FFM calculated as the difference between total body mass and total body fat. Appendicular LST mass was considered equivalent to the sum of LST (i.e., nonfat, nonbone mineral mass) in arms and legs (14, 16). Appendicular LST mass is highly correlated with MRI-derived total body SM mass in healthy adults (13). Appendicular SM represents ~70-80% of total body SM mass (13). The between-measurement technical errors for DEXA fat, FFM, and appendicular LST in the same subject are 3.4, 1.2, and 3.0%, respectively.
Tritium dilution volume. A blood sample was taken before and 3 h after subjects received 0.19 Bq of 3H2O (32). Calculation of 3H2O dilution volume was made after correction for urinary isotope losses. The within-subject technical error for 3H2O dilution volume is 1.5% (28). TBW volume was estimated as the 3H2O dilution space × 0.96, based on correction for nonaqueous hydrogen exchange (30). TBW, in kilograms, was calculated as the product of TBW volume and density at 37°C (0.994 g/cm3).
Whole body 40K counting.
The St. Luke's 4 -whole body counter was used to measure
40K (27). The 40K raw counts
accumulated over 9 min were adjusted for body size on the basis of a
42K calibration equation (29). The
within-subject coefficient of variation in our laboratory for
40K counting is 4% (29). TBK was calculated
as TBK (mmol) = 40K (mmol)/0.000118. BCM was
calculated from TBK as BCM (kg) = 0.00833 × TBK (mmol)
(23).
MRI. Adipose tissue and SM mass were measured using whole body multislice MRI. Subjects were placed on the 1.5 T scanner (General Electric, 6X Horizon, Milwaukee, WI) platform with their arms extended above their heads. The protocol involved the acquisition of ~40 axial images of 10-mm thickness and at 40-mm intervals across the whole body (15, 32). The technical errors for repeated measurements of the same scan by the same observer of MRI-derived SM and adipose tissue volumes in our laboratory are 0.7 and 1.1%, respectively. MRI volume estimates were converted to mass with assumed stable densities for fat and lean tissues (15).
Protein Metabolism
Protein turnover, quantified from the stable isotope [13C]leucine, was evaluated at baseline and after 16 wk of weight loss treatment. A detailed description of the [13C]leucine protein turnover method is provided by Matthews et al. (22). After an overnight fast, the subject was prepared for a 4-h continuous infusion of the stable isotope L-[1-13C]leucine (99% 13C; Mass Trace, Woburn, MA). Tracer was infused through an antecubital vein, and arterialized-venous blood samples were acquired from a contralateral hand vein. Priming doses of sodium [13C]bicarbonate (1.6 µmol/kg FFM) and [1-13C]leucine (4.5 µmol/kg FFM) were administered intravenously, followed by the continuous 4-h infusion of [1-13C]leucine at 4.5 µmol · kg FFMMeasurements of expired air CO2, for 13C
enrichment by isotope ratio mass spectrometry, and pf plasma leucine
and -ketoisocaproate (KIC) 13C enrichments, by gas
chromatography-mass spectroscopy, were performed using methods
previously described (21, 22). The measured plasma [1-13C]leucine and [1-13C]KIC
enrichments as mole % excess 13C and the exhaled
13CO2 enrichments as atom % excess
13C were averaged for each infusion study to produce a
single plateau value. A steady state was defined as a nonsignificant
change in enrichment with time. These values were used to calculate the appearance rate of leucine into plasma, or flux. The only source of
leucine appearance in the postabsorptive state is from protein breakdown; hence, leucine appearance reflects the rate of leucine release from whole body proteolysis (B). The rate of leucine oxidation was also calculated at steady state from the rate of
3CO2 excretion (21,
22). The rate of nonoxidative disposal of leucine at
steady state reflects the uptake of leucine for protein synthesis (S)
and is the difference between the rates of proteolysis and oxidation
(C) in the postabsorptive state: S = B
C. Leucine kinetic
data were calculated on a whole body basis (µmol of leucine/h) and
normalized for metabolic mass as micromoles of leucine per kilogram FFM
per hour.
Statistical Methods
The meanDescriptive changes in the body composition and protein metabolic measures over time were evaluated in the obese women for significance using paired t-tests. Statistical significance was set at P < 0.05.
Data were analyzed using Microsoft Excel Version 5.0 (Microsoft, Redmond, WA). Group subject data are expressed as means ± SD in the text and as means ± SE estimate in Figs. 1 and 2.
![]() |
RESULTS |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Subjects
Obese postmenopausal women.
Sixteen women met the study entry criteria and began weight loss
treatment. There were two early dropouts with poor diet compliance. The
baseline characteristics of the remaining 14 subjects are shown in
Table 1. The subject group consisted of
14 women, 6 African-American and 8 Caucasian, who ranged in age from 56 to 76 yr (mean, 63.4 ± 8.5 yr) at baseline. The group was
moderately obese, with a mean baseline body weight and BMI of 90.1 ± 10.4 kg and 35.2 ± 4.3 kg/m2, respectively. Six
subjects completed the MRI portion of the protocol, and 10 subjects
successfully completed protein turnover studies.
|
|
Reference women.
Forty studies involving a diet restriction-only approach to weight loss
were reported in the meta-analysis of Ballor and Poehlman (1). Subjects were on average young [36.8 ± 1.2 (SE) yr] and obese (88.7 ± 1.9 kg; 42.2 ± 0.8 %fat) women
who on average were calorically restricted for 11.1 ± 0.8 wk. The
group on the whole lost 10.6 ± 0.9 kg of body mass, 2.5 ± 0.3 kg of which was FFM. The ratio FFM/
BW for the group was
0.238 ± 0.022 kg.
Weight Loss Treatment Effects
Body weight and adiposity.
The 14 subjects successfully completed 16 wk of treatment, with a mean
weight loss of 9.6 ± 3.0 kg (P = 0.0001) (Table
1) or 10.7% of initial BW. There were large between-individual
differences in weight loss (Fig. 1),
ranging from a minimum of 6.5% to a maximum of 16.7% of initial BW.
None of the subjects experienced any adverse effects or clinically
important changes over the 16 wk in blood pressure, serum electrolytes,
and serum liver tests; serum lipid levels remained stable or improved
in relation to cardiovascular risk.
|
Lean tissue.
Of the molecular body composition level components, FFM decreased
significantly in the 14 subjects by 2.1 ± 2.6 kg
(P = 0.006) or 19% of weight loss over the 16-wk study
interval (Table 1). The reported relative change with weight loss
treatment for FFM was 2.3 ± 0.7 kg on the basis of the
Ballor-Poehlman ratio of 0.238. The reported and observed FFM values
were not significantly different (P = 0.19) and are
presented in Fig. 2.
|
Protein metabolism.
The results of [13C]leucine kinetic studies are presented
in Table 3. No significant changes in the
rates of leucine flux, oxidation, or synthesis were observed at the end
of the 16-wk weight loss treatment phase.
|
Long-Term Follow-Up
Eleven women returned for follow-up evaluation. The mean follow-up duration was 23.7 ± 5.7 mo with a range of 16-32 mo.The 11 reevaluated women (Table 4)
had a mean body weight at follow-up of 83.0 ± 10.6 kg, which
represents a loss of 3.0 ± 4.9 kg, or a reduction of 3.5% below
their initial body weight (P = 0.033). Of the 11 women,
3 (27%) maintained a weight loss 5% below their baseline level, and
8 (73%) were at weights that ranged between 97 and 104% of their
respective baseline levels. None of the women reported intervening
weight loss treatment. The group's mean weight increased by 5.4 ± 4.3 kg between the second and third follow-up visits.
|
Fat mass in the reevaluated group was 2.4 ± 4.2 kg (6.0%) below baseline values (P = 0.043) and represented 78% of weight loss.
FFM, appendicular LST mass, and BCM were nonsignificantly changed from their baseline levels by 0.7 ± 1.6 kg (P = 0.09), 0.3 ± 0.8 kg (P = 0.12), and 0.02 ± 2.1 kg (P = 0.49), respectively (Table 4). There was a nonsignificant change in bone mineral mass of 0.043 ± 0.145 kg. The loss of FFM (0.7 ± 1.6 kg) was not significantly different from that reported (0.7 ± 1.1) (P = 0.41).
![]() |
DISCUSSION |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Composition of Weight Loss
The principal finding of this study was that prescribed weight loss in obese postmenopausal women consisted of a small and appropriate amount of FFM relative to that in young dieting women. This observation, based on a small but thoroughly evaluated cohort, fails to support any adverse effect of dieting on LSTs in postmenopausal women. Our study also provides two additional observations in support of this conclusion on the basis of FFM. First, we quantitatively explored losses of other related components, such as SM, appendicular LST, BCM, and TBW. Although all of these components were lost to varying degrees with weight loss, none changed in a manner contradictory to known body composition relationships. Second, we did not observe any relative changes in leucine metabolism suggestive of undue catabolic weight loss effects. This observation supports the minimal LST effects of dieting in the postmenopausal women whose relatively small losses of protein-containing tissues, such as SM mass, fail to support a large weight loss-induced period of negative nitrogen balance. Thus, taken collectively, weight loss with a hypocaloric diet in our postmenopausal obese women was not accompanied by unduly large or disproportionate losses of functionally important body composition compartments (40).When the mean 2-yr follow-up results in these women are considered,
there likely exists the additional small aging-related lean tissue loss
anticipated from previous cross-sectional (5, 14, 25, 26) and longitudinal
(10) aging studies. The observed FFM reduction over 2 yr
in these older women undoubtedly includes an aging-related portion in
addition to that accounted for solely by body mass change. Although
these two separate portions of FFM cannot be identified in the
present study, the actual
FFM was relatively modest (0.7 kg) and
equivalent to that reported for weight loss alone.
There was an absence of significant bone mineral change over 16 wk of weight loss treatment or 2 yr of follow-up, even though there were weight and age changes in a direction associated with gradual depletion of bone mass (31). None of our subjects was actively engaged in physical activity programs or was taking estrogen replacement therapy, measures that might prevent loss of bone mineral (18, 24). The 16-wk post-weight-loss evaluation may have been too short a period, and a sample of 14 women may not have been large enough to detect the expected small changes in bone mineral mass (31).
The phenomenon of separate changes in bone mineral and other LSTs requires a careful consideration of our developed FFM and other prediction models. For example, the fraction of FFM as water is usually reported as ranging between 0.70 and 0.75. However, the FFM hydration of ~0.70 assumes that the fraction of FFM as bone mineral is also relatively stable (37). On the other hand, the water fraction of most fat-free soft tissues approximates ~0.80 (17, 35). This may partly explain why our observed change in water relative to FFM was higher than expected (0.86). Subtle effects, such as those noted with a lack of bone mineral loss, may cause small deviations from the change expected.
An intentional aspect of our protocol was to evaluate the effects on body composition of a nutritionally adequate hypocaloric diet. Physical activity as part of treatment was discouraged. To what extent exercise regimens might reduce lean tissue losses remains unclear (34). A small positive increment in the fraction of weight loss as fat is recognized with weight loss treatment combined with structured exercise programs (1, 12). Moreover, strength training of elderly women results in small increases in SM mass and large relative improvements in strength (9, 24). The addition of an aerobic exercise program to a hypocaloric diet in obese older men failed to attenuate the loss in FFM (6, 7).
In addition to monitoring component changes over time, our analysis included baseline and 16-wk follow-up assessment of leucine kinetics. No significant changes at the 16th wk of dieting were detected in fasting leucine flux, synthesis, or oxidation, an observation consistent with the relatively small FFM and other nonosseous component (i.e., protein) losses. Our sample size was small, and thus our power to detect subtle changes in protein metabolism with weight loss was limited. Future studies with larger numbers of subjects and age distributions are needed to extend the present study observations.
The nonlean tissue components of body mass change with dieting included
substantial losses of both subcutaneous (16.6%) and visceral adipose
tissue (
25%). Adipose tissue and closely related fat mass accounted
for 79 and 80% of the observed weight loss at 16 wk of treatment and 2 yr of follow-up, respectively. The diet-induced weight loss of ~8.2
kg corresponded to a 25% reduction in visceral adipose tissue in this
sample. Given that a strong association has been reported in a
similarly aged cohort between abdominal adiposity and risk of stroke
(11) in terms of body composition, the goal of losing body
fat, particularly in the visceral compartment, was accomplished in
these elderly women.
Weight Loss Program
Our subjects lost ~10% of their baseline BW after 16 wk of treatment and, of those reevaluated at 2 yr of follow-up (11/14 subjects), 35% of the mean weight loss was maintained. This level of weight maintenance is within the range reported for other 1- and 2-yr diet-behavioral studies (2, 19). Our findings of primarily loss of body fat (i.e., ~80% of weight loss) with dieting in elderly women provides strong support for advancing obesity studies in this population from an exploratory to an intensive analysis level.Prescribing weight loss treatment for older individuals raises an important and unresolved question of efficacy. A recent study reported increased associations between higher body weights/adiposity and lower levels of physical functioning (e.g., climbing stairs and moderate activities), lower feelings of well being, and a greater burden of pain among middle-aged and older women (4). However, a growing literature reports a failure to clearly link higher levels of BMI in older individuals with greater morbidity and mortality risk (3, 36). Thus, it remains unclear whether older subjects, even if successful weight losers and maintainers, would experience any clinical or health benefits from their efforts.
Conclusion
The focus of this study was to quantify body composition effects in an elderly cohort of obese women after ingestion of a hypocaloric diet. The present investigation provides a comprehensive analysis of weight loss composition observed in nonexercising obese dieting elderly women who were subsequently followed for a mean of 2 yr. Our findings suggest that a small and appropriate fraction of weight loss consists of soft lean tissues including FFM and SM, whereas the majority of observed weight loss is fat. Elderly women who diet, even in the absence of vigorous exercise training, experience body composition changes that are generally recognized as beneficial. Important functional and clinical issues await resolution on the basis of larger, possibly longer, and appropriately controlled prospective studies. ![]() |
ACKNOWLEDGEMENTS |
---|
This study was supported in part by National Institutes of Health Grants F32-AG-05679, R29-AG-14715, RR-00645, and DK-42618.
![]() |
FOOTNOTES |
---|
Address for reprint requests and other correspondence: D. Gallagher, Obesity Research Center, 1090 Amsterdam Ave., New York, NY 10025 (E-mail: dg108{at}columbia.edu).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.
Received 27 July 1999; accepted in final form 8 February 2000.
![]() |
REFERENCES |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
1.
Ballor, DL,
and
Poehlman ET.
Exercise-training enhances fat-free mass preservation during diet-induced weight loss: a meta-analytical finding.
Int J Obes
18:
35-40,
1994[ISI].
2.
Bartlett, SJ,
Faith MS,
Fontaine KS,
Cheskin LJ,
and
Allison DB.
Is the prevalence of successful weight loss and maintenance higher in the general community than the research clinic?
Obes Res
7:
407-413,
1999[Abstract].
3.
Bender, R,
Jocker KH,
Trautner C,
Spraul M,
and
Berger M.
Effect of age on excess mortality in obesity.
JAMA
281:
1498-1504,
1999
4.
Coakley, EH,
Kawachi I,
Manson JE,
Speizer FE,
Willet WC,
and
Colditz GA.
Lower levels of physical functioning are associated with higher body weight among middle-aged and older women.
Int J Obes
22:
958-965,
1998[ISI].
5.
Cohn, SH,
Vaswani A,
Aloia JF,
Roginsky M,
Zanzi I,
and
Ellis KJ.
Changes in body chemical composition with age measured by total body neutron activation.
Metabolism
26:
85-96,
1976.
6.
Dengel, RD,
Hagberg JM,
Coon PJ,
Drinkwater DT,
and
Goldberg AP.
Effects of weight loss by diet alone or combined with aerobic exercise on body composition in older obese men.
Metabolism
43:
867-871,
1994[ISI][Medline].
7.
Dengel, RD,
Hagberg JM,
Coon PJ,
Drinkwater DT,
and
Goldberg AP.
Comparable effects of diet and exercise on body composition and lipoproteins in older men.
Med Sci Sports Exerc
26:
1307-1315,
1994[ISI][Medline].
8.
Dutta, C,
and
Hadley EC.
The significance of sarcopenia in old age.
J Gerontol
50A:
1-4,
1995[ISI].
9.
Fiatarone Singh, MA,
Ding W,
Manfredi TJ,
Solares GS,
O'Neill EF,
Clements KM,
Ryan ND,
Kehayias JJ,
Fielding RA,
and
Evans WJ.
Insulin-like growth factor I in skeletal muscle after weight-lifting exercise in frail elders.
Am J Physiol Endocrinol Metab
277:
E135-E143,
1999
10.
Flynn, MA,
Nolph GB,
Baker AS,
Martin WM,
and
Krause G.
Total body potassium in aging humans: a longitudinal study.
Am J Clin Nutr
50:
713-717,
1989[Abstract].
11.
Folsom, AR,
Prineas RJ,
Kaye SA,
and
Munger RG.
Incidence of hypertension and stroke in relation to body fat distribution and other risk factors in older women.
Stroke
21:
701-706,
1990[Abstract].
12.
Forbes, GB.
Human Body Composition. New York: Springer-Verlag, 1987.
13.
Gallagher D, Heymsfield SB, and Wang Z. Skeletal muscle markers.
In: The Role of Protein and Amino Acids in Sustaining and
Enhancing Performance, by the Institute of Medicine. Washington,
DC: National Academy Press, 1999, p. 255-277.
14.
Gallagher, D,
Visser M,
De Meersman RE,
Sepulveda D,
Baumgartner RN,
Pierson RN,
Harris T,
and
Heymsfield SB.
Appendicular skeletal muscle mass: effects of age, gender, and ethnicity.
J Appl Physiol
83:
229-239,
1997
15.
Heymsfield, SB,
Ross R,
Wang ZM,
and
Frager D.
Imaging techniques of body composition: advantages of measurement and new uses.
In: Emerging Technologies for Nutrition Research. Washington, DC: National Academy Press, 1997, p. 127-150.
16.
Heymsfield, SB,
Smith R,
Aulet M,
Bensen B,
Lichtman S,
Wang J,
and
Pierson RN.
Appendicular skeletal muscle mass: measurement by dual-photon absorptiometry.
Am J Clin Nutr
52:
214-218,
1990[Abstract].
17.
Institute of Medicine.
Weighing the Options: Criteria for Evaluating Weight-Management Programs. Washington, DC: National Academy Press, 1995.
18.
Kiel, DP,
Felson DT,
Anderson JJ,
Wilson PWF,
and
Moskowitz MA.
Hip fracture and the use of estrogens in postmenopausal women: the Framingham Study.
N Engl J Med
317:
1169-1174,
1987[Abstract].
19.
Klem, ML,
Wing RR,
McGuire MT,
Seagle HM,
and
Hill JO.
A descriptive study of individuals successful at long-term maintenance of substantial weight loss.
Am J Clin Nutr
13:
326-331,
1994.
20.
Kuczmarski, RJ,
Flegal KM,
Campbell SM,
and
Johnson CL.
Increasing prevalence of overweight among US adults.
JAMA
272:
205-211,
1994[Abstract].
21.
Matthews, DE.
Stable isotope methodologies in studying human amino acid and protein metabolism.
Ital J Gastroenterol
25:
72-78,
1993[ISI][Medline].
22.
Matthews, DE,
Motil KJ,
Rohrbaugh DK,
Burke JF,
Young VR,
and
Bier DM.
Measurement of leucine metabolism in man from a primed, continuous infusion of L-[l-13C]leucine.
Am J Physiol Endocrinol Metab
238:
E473-E479,
1980
23.
Moore, FD,
Olsen KH,
McMurray JD,
Parker HV,
Ball MR,
and
Boyden CM.
The Body Cell Mass and Its Supporting Environment: Body Composition in Health and Disease. Philadelphia, PA: Saunders, 1963.
24.
Nelson, MA,
Fiatarone MA,
Morganti CM,
Trice I,
Greenberg RA,
and
Evans WJ.
Effects of high-intensity strength training on multiple risk factors for osteoporotic fractures.
JAMA
272:
1909-1914,
1994[Abstract].
25.
Novak, LP.
Aging, total body potassium, fat-free mass, and cell mass in males and females between ages 18 and 85 years.
J Gerontol
27:
438-443,
1972[ISI][Medline].
26.
Oberhausen, E,
and
Onstad CO.
Relationship of potassium content of man with age and sex.
In: Radioactivity in Man, edited by Meneely GR,
and Linde SM. Springfield, IL: Thomas, 1995, p. 179-202.
27.
Pierson, RN,
Lin DHY,
and
Phillips RA.
Total body potassium in health: effects of age, sex, height, and fat.
Am J Physiol
226:
206-212,
1974[ISI][Medline].
28.
Pierson, RN,
Wang J,
Colt EW,
and
Neumann P.
Body composition measurements in normal man: the potassium, sodium, sulfate, and tritium spaces in 58 adults.
J Chronic Dis
35:
419-428,
1982[ISI][Medline].
29.
Pierson, RN, Jr,
Wang J,
Thornton JC,
Van Itallie TB,
and
Colt EW.
Body potassium by 4- 40K counting: an anthropometric correction.
Am J Physiol Renal Fluid Electrolyte Physiol
246:
F234-F239,
1984[ISI][Medline].
30.
Racette, SB,
Schoeller DA,
Luke AH,
Shay K,
Hnilicka J,
and
Kushner RF.
Relative dilution spaces of 2H- and 18O-labeled water in humans.
Am J Physiol Endocrinol Metab
267:
E585-E590,
1994.
31.
Ricci, TA,
Chowdhury HA,
Heymsfield SB,
Stahl T,
Pierson RN,
and
Shapses SA.
Calcium supplementation suppresses bone turnover during weight reduction in postmenopausal women.
J Bone Miner Res
13:
1045-1050,
1998[ISI][Medline].
32.
Ross, R,
Léger L,
Morris D,
De Guise J,
and
Guardo R.
Quantification of adipose tissue by MRI: relationship with anthropometric variables.
J Appl Physiol
72:
787-795,
1992
33.
Ryan, AS,
Nicklas BJ,
and
Dennis KE.
Aerobic exercise maintains regional bone mineral density during weight loss in postmenopausal women.
J Appl Physiol
84:
1305-1310,
1998
34.
Ryan, AS,
Pratley RE,
Elahi D,
and
Goldberg AP.
Resistive training increases fat-free mass and maintains RMR despite weight loss in postmenopausal women.
J Appl Physiol
79:
818-823,
1995
35.
Snyder, WS,
Cook MJ,
Nasset ES,
Karhausen LR,
Howells GP,
and
Tipton IH.
Report of the Task Group on Reference Men.
In: International Commission on Radiological Protection No. 23. Oxford, UK: Pergamon, 1975.
36.
Stevens, J,
Cai J,
Pamuk ER,
Williamson DF,
Thun J,
and
Wood JL.
The effect of age on the association between body-mass index and mortality.
N Eng J Med
338:
1-7,
1998
37.
Wang, Z,
Deurenberg P,
Wang W,
Pietrobelli A,
Baumgartner RN,
and
Heymsfield SB.
Hydration of fat-free body mass: review and critique of a classic body-composition constant.
Am J Clin Nutr
69:
833-841,
1999
38.
Wang, Z,
Pierson RN,
and
Heymsfield SB.
The five level model: a new approach to organizing body composition research.
Am J Clin Nutr
56:
19-28,
1992[Abstract].
39.
Watkins, JC,
Roubenoff R,
and
Rosenberg IH
(Editors).
Proceeding from a Conference on Body Composition: The Measures and Meaning of Changes With Aging Tufts University, Nov. 6-7, 1991. (USDA)
40.
Webster, JD,
Hesp R,
and
Garrow JS.
The composition of excess weight in obese women estimated by body density, total body water, and total body potassium.
Hum Nutr Clin Nutr
38:
299-306,
1984[Medline].
41.
Weir, JBV
New methods for calculating rate with special reference to protein metabolism.
J Physiol (Lond)
109:
1-9,
1949[ISI].