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8 AUTHORS, INCLUDING:
Friedl, Karl E., Robert J. Moore, Lester E. Martinez- tended consequence of severe dietary practices, and it is
Lopez, James A. Vogel, E. Wayne Askew, Louis J. Mar- the accidental status of some displaced and famine-
chitelli, Reed W. Hoyt, and Claire C. Gordon. Lower limit stricken populations in an early stage of food depriva-
of body fat in healthy active men. J. Appl. Physiol. 77(Z): 933- tion.
940,1994.-We examined body composition changes in 55 nor-
mal young men during an 8-wk Army combat leadership train- The quantification of a minimum BF in humans has
ing course involving strenuous exercise and low energy intake, been elusive because of deviations from the normal as-
with an estimated energy deficit of 5.0 t 2.0 MJ/day and a sumptions of various chemical models at this extreme
resultant 15.7 k 3.1% weight loss. Percent body fat (BF) mea- end of body composition. Thus, in one study of lipodys-
sured by dual-energy X-ray absorptiometry (DEXA) averaged trophy patients, three black women all produced spuri-
14.3% (range 6-26%) and 5.8 t_ 1.8% (range 4-11%) at the be- ous negative percent BF estimates from hydrodensitome-
ginning and end of the course, respectively. Men who achieved try, even though adipose tissue was visualized by mag-
a minimum percent BF (4-6%) by 6 wk demonstrated only netic resonance imaging (9). Another woman assessedby
small additional total and subcutaneous fat losses in the final 2 body water dilution with H,180 and with the tenuous as-
wk and sacrificed increasingly larger proportions of fat-free sumption that 73% of the nonfat body weight is water
mass. Percent BF estimated from skinfold thicknesses re-
flected relative changes in fat mass, although actual percent BF yielded 3% BF (21). After 24 wk of semistarvation with a
was overestimated. Instead of reaching a plateau after fat 25% reduction in body weight in the Minnesota study,
stores were substantially depleted, abdominal, hip, and thigh underwater weighing of several individuals yielded den-
girths continued to decline with body weight loss. Final percent sity values that equaled or exceeded the density normally
BF for the leanest men was similar to that observed after a 25% assumed for a fat-free mass (FFM) component (1.100
body weight reduction in the 1950 Minnesota study (5.2% by g/cm3) (19). An attempt to correct the normally assumed
underwater weighing), and height-corrected final fat mass was density of the FFM for estimated increases in the frac-
the same (1.0 k 0.2 vs. 0.9 t 0.7 kg fat/m2), suggesting that tional contributions of both bone and water approxi-
these values represent a minimal body fat content in healthy mately cancelled out each other. Anthropometric assess-
men and that weight loss subsequent to achieving this level is
contributed from the fat-free mass. Our results suggest that ments of BF that have been established by comparison to
4-6% BF or ~2.5 kg fat represents the lower limit for healthy hydrodensitometry consistently overestimated lean indi-
men, as assessed by DEXA or by underwater weighing. viduals (36).
The more recently developed dual-energy X-ray ab-
densitometry; anthropometry; weight reduction; body compo- sorptiometry (DEXA) technology (24) provides another
sition; energy expenditure opportunity to assess extremes of body composition.
This appears to be a promising approach to defining the
lower limits of BF because bone mineral content is sepa-
ATYPICALFITYOUNGMALE hasbody fat(BF)storesto- rately assessed,eliminating this confounder. Validation
taling 15% body weight or - lo-11 kg. This represents a studies have demonstrated high correlations between
compact energy store of - 100,000 kcal, equivalent to dual-photon absorptiometry (closely related to DEXA)
230 kg of glycogen. These energy stores are progressively and criterion methods including hydrodensitometry (15),
diminished during a chronic energy deficit and approach and mixtures of porcine lard and lean ox thigh produced
a minimum level beyond which protein catabolism neces- a high linear correlation with DEXA across a broad span
sarily increases (4,7,19). In some species where an insu- of soft tissue composition (1.3~87.6%) (13). In our labora-
lating layer of blubber is essential to survival, such as the tory, DEXA estimates of percent BF are well correlated
elephant seal and king penguin, significant protein catab- with hydrodensitometry for young men [r = 0.90, stan-
olism occurs during starvation even when large amounts dard error of estimate (SEE) = 2.94, n = 551 and women
of fat are present (27). Humans do not appear to spare (r = 0.91, SEE = 3.15, n = 48).
subcutaneous fat at the expense of body protein and, on We examined the lower limits of BF measured by
the basis of studies of lipodystrophy patients, survive DEXA and anthropometry in a group of healthy young
with only a miniscule amount of fat. This minimal or men who lost >lO% of body weight over 8 wk and re-
“essential” fat that is consistent with life represents the mained highly active in the face of a large energy deficit
lipid components of cell membranes, nerve sheaths, and while participating in an 8-wk Army Ranger course. Food
other cellular constituents, with adipose tissue serving deprivation is a deliberate stressor in this voluntary
important mechanical functions in at least a few critical combat leadership course, but recent changes in the
areas such as within the orbits and on the palms and course structure had inadvertently increased the energy
soles (9). This condition where minimum fat coexists deficit to a level excessive to the objectives of the course.
with still relatively normal amounts of skeletal muscle is We report data for a group of men who represent an
observed in some body builders and wrestlers as an in- extreme level of energy deprivation and weight loss that
933
934 LOWER LIMIT OF BODY FAT
appears to rest on the edge between a minimum achiev- TABLE 1. Initial physical characteristics of a Ranger
able BF and a point beyond which food cravings and un- class and a previously studied group of combat engineers
acceptable losses of muscle mass would have ended vol-
untary participation. Ranger Class
Baseline 2 wk 4 wk 6 wk 8 wk
Values are means -t SD; n = 55 men. Intervals between testing periods are baseline-2 wk, 15 days; 2-4 wk, 17 days; 4-6 wk, 16 days; 6-8 wk, 14
days. NM, not measured due to time limitations. Different symbols indicate significantly different means (Scheffe’s test; P < 0.05).
936 LOWER LIMIT OF BODY FAT
half of the group was double that of the other half (40 t 10
Baseline
11 vs. 18 t 8%). When subdivided to the leanest quartile
of men, FFM loss accounted for ~50% of the weight loss 8.
achieved by 6 wk and 60% of all weight lost by the end of
the course.
6'
Comparison of gravimetrically based and DEXA-as-
sessedweights. Mean fat mass detected by DEXA was
nearly identical to the mass calculated from body weight 4-
I
. - .1.1 ‘>
obtained on any individual was 3.8% BF. By all indica-
2ov
?.??
--CI
Fat loss - six weeks
tions, 2.5 kg of fat mass (or -4% body weight) represents
, Fat loss - last 2 wk
a physiological lower limit in healthy men (Fig. 3). At the
i m Remaining fat
ip ___-... . .---_ end of the Ranger course, skinfold thicknesses had ap-
proached a minimum (total of 4 skinfolds ~20 mm) in the
men who were leanest at the start of the course (~10%
BF). Body fat did not appreciably decline in these men
during the final 2 wk of the course, and their predomi-
nant source of energy from body stores (by weight) came
from components of the FFM. As in the Minnesota study
(3l), this level of food restriction also approached the
voluntarily tolerable limit for even highly motivated
men. Thus, even though all of the soldiers understood
the rules of the course, two of the leanest men from our
original study group were failed because they obtained
unauthorized food in the final week of their evaluation;
unfortunately, final data could not be obtained on
these two.
In contrast to two-compartment evaluations of body
composition that rely on assumptions about the homoge-
neity of the fat-free component, DEXA estimates the fat
and fat-free tissue solely on the basis of the soft tissue
pixels (interpolating the composition and quantity of
soft tissue in bone-containing pixels), eliminating any
bV -16 A.._-_.-_-u-m- _., -.- _____ ._--
error due to differences in the fractional contribution of
6
Individuals, by initial fat weight bone mineral to the FFM. Such an error becomes impor-
tant as lean tissue other than bone is catabolized during a
3. Individual
FIG. fat mass at start, 6 wk, and end of Ranger train- progressive weight loss and the density of the remaining
ing (top). Bottom: change in fat-free mass for same individuals. n = 55.
* Five men who were not measured at 6 wk. FFM increases. Even though DEXA is an improvement
over methods such as underwater weighing because of
value in the original test population of Durnin and Wo- the actual assessment of bone separately from the soft
mersley. tissue, the method is still dependent on assumptions
about the composition of the representative lean tissue
against which the r values are compared. Large weight
DISCUSSION
reductions involving primarily fat mass in massively
After 8 wk of sustained high activity and a substantial obese subjects appear to be properly assessedby the simi-
shortfall in energy intake, the volunteers in our study lar dual-photon absorptiometry devices (22), but an ex-
averaged 5.8% BF by DEXA. The lowest measurement amination of weight loss involving a substantial loss of
critical consideration, and even for nonobese individuals, provides an accurate reflection of total BF stores even at
differences in nutritional status will have a significant this extreme, even though problems have been encoun-
impact on the final outcome. For example, the weights of tered when using skinfold thicknesses to demonstrate
1,200 semistarved British and Indian soldiers were fol- large fat reductions at the other extreme of fatness in
lowed carefully during the Turkish siege of Kut, where it obese patients (2, 30) and when the change is in the op-
was noted that the men who began with a “superabun- posite direction, during refeeding of malnourished
dance of fat” were able to withstand the loss of lo-14% of men (32).
body weight, whereas other men, primarily the Indian Eight of the men in this study were again tested by
soldiers who began with a smaller fat reserve, readily DEXA 6 mo after the end of their training, and values of
died in the cold temperatures of a southern Mesopota- lean mass and fat mass were nearly identical to their
mian winter (14). The US Army Ranger School has de- starting values. During the course, body weights declined
termined through experience that wintertime Ranger from 76.0 t 11.4 to 63.5 t 8.6 kg and 6 mo later averaged
classes require more food to meet energy demands, and 77.4 t 11.2 kg (25). H owever, soldiers completing this
students typically receive 11.7 MJ/day on the days that training report an interim period of fat mass rebound
summertime students receive restricted rations of 5.4 and intensive refeeding that peaked l-2 mo after the
MJlday. course. This has been measured in a second study and
Extreme differences in the response to energy deficit averages -150% of the fat mass of the original measure,
between individuals were demonstrated by two of the with the largest increase in abdominal circumference
leanest individuals who completed the study. They both (unpublished data).
started at 6-8% BF, 75-77 kg body weight, and a body In summary, 4-6% BF or -2.5 kg of BF appears to be
mass index of 24.5 kg/m2 and completed the course at the minimum BF achievable in healthy men. This corre-
4-5% BF, but one weighed 69 kg (-9.0% of initial body sponds to a sum of four skinfolds <20 mm. In fit and
weight) and the other weighed 59 kg (-23.4% of initial well-nourished young American men averaging 15% BF,
body weight). These two men bracketed the full range of the rapid loss of 16% of body weight leads to a virtual
relative weight loss observed in this study. The young depletion of fat stores, i.e., fat other than “essential fat.”
soldier with the highest weight loss also achieved the Because this is also the point at which the individuals
highest FFM loss (13.8 kg of initial FFM, or -40% of his enter a phase of increased muscle catabolism, this is an
total muscle mass). Thus, relative to the other men, one excessive weight loss for healthy young men. Large
was remarkable for his ability to adapt to the restricted changes in neck and thigh circumference are markers of
energy intake and the other was remarkable for his fail- this increased catabolism, whereas skinfolds are good
ure to adapt. This highlights the difficulty of modeling markers of the reduction in BF, as are waist and hip
weight loss due to restricted energy intake, especially in circumferences.
the absence of direct measurements or better predictors
of individual metabolic responses (12, 28). We are grateful to Robert Petrin, Sgt. Kong Ang, Maj. Barry Fair-
brother (Royal Logistics Corps, UK), S. Sgt. Glenn Thomas, Elaine
The pattern of changes in skinfold thicknesses and Christensen, and Spc. Sherry1 Kubel for dedication and skilled work in
body circumferences supports the notion that truncal fat this study. We thank Dr. John Patton for careful review of earlier
stores are the primary energy supply even for relatively drafts of this manuscript. We are most indebted to the men who agreed
lean young men (3). The abdominal girth decreased more to participate in this study, over and above the extreme demands of
than the girth of the hips, probably reflecting the use of Ranger training. This study was performed at the request of Col. John
Maher III, Commander of the IJS Army Ranger Training Brigade.
intra-abdominal as well as subcutaneous fat. Abdominal The opinions or assertions contained herein are the private views of
girths continued to decline almost in a linear fashion to the authors and are not to be construed as reflecting the official views
the end of the course, clearly reflecting lean tissue as well of the Department of the Army or Department of Defense.
as fat loss from this area in the later stages of the course. This work was presented at American Association for the Advance-
ment of Science Symposium “Humans Under Stress: Will They Sur-
A previous study of Norwegian cadets in a Ranger train-
vive?” at the Institute of Environmental Stress, Santa Barbara, CA, on
ing program with 1 wk of complete food and sleep depri- June 21-25, 1992.
vation demonstrated emptying of abdominal and gluteal Address for reprint requests: K. E. Friedl, SGRD-PLC, HQ, US
adipocytes with little change in femoral fat (29). How- Army Medical Research & Development Command, Fort Detrick, MD
ever, in our protracted period of energy deficit, there was 217025012.
a startling decline in the girth of even the thigh, repre- Received 26 July 1993; accepted in final form 4 April 1994.
senting even a slightly greater proportional reduction in
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