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1Military Performance Division, 2Thermal and Mountain Medicine Division, 3Military Nutrition Division, United States Army Research Institute of Environmental Medicine, Natick, Massachussetts 01760; 4Diagnostic Systems Laboratories Canada, and 5Department of Laboratory Medicine and Pathobiology, University of Toronto and Mount Sinai Hospital, Toronto, Canada M5G 1X5
Submitted 12 December 2002 ; accepted in final form 19 May 2003
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ABSTRACT |
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 TOP ABSTRACT METHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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-hydroxybutyrate), and body composition were measured in 12 men (22
± 3 yr, 87 ± 8 kg, 183 ± 7 cm, 20 ± 5% body fat)
on days 1, 3, and 4 during a control and experimental (Exp)
period. During Exp, subjects performed prolonged work (energy expenditure of
4,500 kcal/day) with caloric (1,600 kcal/day) and sleep (6.2 h total)
restriction. IGF-I and IGFBP-3 were measured by immunoassay before and after
immunoaffinity depletion of ALS-based complexes (i.e., ternary complex
removal). Exp produced losses in body mass (-3.0%), lowered total IGF-I
(-24%), free IGF-I (-42%), IGFBP-3 (-6%), nonternary IGF-I (-27%), and IGFBP-3
(-16%), and increased IGFBP-1 (256%). No Exp effects were observed for ALS. No
changes were observed in the proportion of IGF-I circulating in free
(1.2%), ternary (87.4%), or nonternary (11.4%) molecular
complexes. During Exp, glucose concentrations were lower on day 3,
but days 1 and 4 were statistically similar. In conclusion,
during a short-term energy deficit in young, healthy men, 1) IGF-I
system components differentially respond (both in direction and magnitude) to
a given metabolic perturbation and 2) the relative proportion of
IGF-I sequestered in ternary vs. nonternary molecular complexes appears to be
well maintained. somatotropic hormones; nutritional status; binary concentrations; magnetic exclusion separation; fasting
More than 75% of IGF-I circulates in a 150-kDa ternary complex comprised of IGF-I, IGFBP-3, and an acid labile subunit (ALS), with smaller proportions circulating in a 30- to 50-kDa binary (IGF-I bound to one of its smaller molecular mass BPs) or free forms (16, 37, 40). The physiological relevance of assessing nonternary concentrations resides in the fact that IGF-I complexed in ternary form cannot pass out of the vascular space, whereas the binary and free IGF-I forms can pass through the capillary fenestrations and bind to cell surface receptors. IGF-I possesses substantial hypoglycemic effects (5), but the ternary complex affects the amount of IGF-I available to alter glucose uptake. Changes in IGFBPs within the hormonal milieu are presumed to induce a shift in the relative proportion of ternary vs. binary forms of IGF-I, yet few investigations have directly evaluated this hypothesis.
A major environmental factor influencing IGF-I concentrations is nutritional status (2, 4, 9, 19, 20, 36, 40). Caloric and protein restriction can reduce IGF-I gene expression and circulating IGF-I and IGFBP concentrations (8, 13, 33). In studies that characterized the long-term (i.e., 8 wk) physiological responses to military operational stress (prolonged physical exertion, and caloric and sleep restriction) (11), IGF-I declined abruptly and remained low until the combined stressors were removed, and the magnitude of IGF-I decline was indirectly related to the magnitude of body mass loss. Accompanying the decline in IGF-I during military operational field training are losses of lean body mass, decreased lymphocyte proliferation, and greater insulin resistance (11, 27). How IGFBPs respond to this multistressor environment and its impact on IGF-I availability have not been studied.
This study examined the hypothesis that military operational field training (sustained physical activity and sleep deprivation superimposed on a short-term energy deficit) would alter IGFBPs and alter the proportion of IGF-I circulating in ternary vs. binary molecular complexes. The specific objectives of this study were to 1) assess IGF-I and IGFBP temporal responses during 3 days of sustained physical exertion combined with food and sleep restriction, 2) employ a novel magnetic separation procedure to measure nonternary (i.e., binary) IGF-I and IGFBP-3 concentrations, and 3) examine the relationship between changes in the IGF-I system and other traditional markers of metabolic status.
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METHODS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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Experimental approach. A repeated-measures within-subject design was used to study alterations in IGF-I system components and biomarkers of nutritional status during 3 days of military operational stress. The study was conducted over a 2-wk period. During week 1 (control), morning (0630) fasted blood was obtained on days 1, 3, and 4. Week 2 was the experimental week (Exp) during which morning fasted blood was also sampled on days 1 (before the subjects were exposed to the experiment), 3, and 4 during sustained operations (SusOps). During Exp, the soldiers completed field training, which consisted of a variety of military-relevant tasks and skills training. Physical activity and movement were recorded every minute by a wrist-worn actigraph (Mini Mitter, Bend, OR, and Precision Control Designs, Ft. Walton Beach, FL) to quantify amount of sleep obtained during Exp. Time sleeping was calculated by summing the number of minutes whose signal was zero or when at background levels. Food and sleep restriction and sustained physical exertion were deliberate stressors during the training. Caloric intake was restricted to one meal ready to eat plus either a small breakfast (bagel, juice, and fruit) or a snack each day. The caloric and nutritional composition of the daily rations were calculated from the meal ready to eat version and menu consumed, manufacturer supplied labels, and American Diabetes Association Exchange values (see Table 1). Sleep was restricted by only scheduling two 1-h blocks of sleep a day and keeping the soldiers busy performing mental and physical tasks for the majority of each day. The level of caloric restriction, sleep deprivation, and prolonged work were chosen to model "real-world" scenarios expected by the US military in combat situations. The physical activity of the military training could be regarded as very light (map reading, etc.) to very high (confidence course, repetitive box lifting, etc.). The major contributor to energy expenditure was sustained aerobic exercise associated with nightly road marches, land navigation, and patrolling activities (estimated exercise intensity of 30-40% maximal oxygen consumption). Other results from this research study have been published elsewhere (7, 30).
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Dual-energy X-ray absorptiometry. Body composition was assessed by whole body dual-energy X-ray absorptiometry (DXA). Total body estimates of %body fat, bone mineral density, and bodily content of bone, fat, and nonbone lean tissue were determined by using manufacturer-described procedures and supplied algorithms (Total Body Analysis, version 3.6, Lunar, Madison, WI). Precision of this measurement is better than ±0.5% body fat (27). Scanning was in 1-cm slices from head to toe by using the 20-min scanning speed. Subjects had DXA scans performed before and the morning after the study.
Blood collection. At 0630 on days 1, 3, and 4 of control and Exp, morning fasting blood samples were obtained by venipuncture. Blood was allowed to clot at room temperature and was centrifuged for 30 min at 3,000 g at 4°C. After centrifugation, serum was aliquoted into an appropriate storage vial, flash frozen in liquid nitrogen, and stored at -80°C for later analysis. To eliminate interassay variances, all samples were assayed within the same batch.
IGF-I system assays. Total IGF-I, free IGF-I, IGFBP-1, and IGFBP-3 concentrations were determined by a two-site immunoradiometric assay (Diagnostic System Laboratories, Webster, TX). The sensitivity of these assays were 2.06, 0.03, 0.33, and 0.05 ng/ml for total IGF-I, free IGF-I, IGFBP-1, and IGFBP-3, respectively. The intra-assay variances for the immunoradiometric assay were all <5.3%. IGFBP-2 concentrations were determined by a radioimmunoassay (Diagnostic Systems Laboratories). The sensitivity of this assay was 0.05 ng/ml. The intra-assay variance was <6.2%.
To determine the extent of the nonternary (i.e., binary) association, IGF-I and IGFBP-3 were also measured by the Diagnostic Systems Laboratory (DSL) IGF-I and IGFBP-3 methods after immunoaffinity depletion of the ALS-based complexes, as previously described (21). Briefly, a predetermined amount of anti-ALS antibody (DSL) was coupled to a streptavidin-coated magnetic particle and used for immunodepletion of the ALS-based complexes. An optimized amount of the antibody-coupled particles (300 µl of 1 mg/ml particle suspension) was added to polystyrene tubes (12 x 75 mm), and the tubes were placed onto the magnetic separation rack to side-separate the particles and completely remove the particles' suspension buffer. To each tube was then added 20 µl of the serum samples and 20 µl of the assay buffer, which was allowed to incubate for 2 h with continuous shaking. The tubes were then placed on the magnetic separation rack, and the ALS-depleted samples were assayed for IGF-I and IGFBP-3, as well as ALS, to ensure complete removal of the ALS immunoreactivity. In addition, the efficiency of ALS removal was assessed by analyzing acromegalic samples with high ALS content and showing the efficiency of the method for removing >99% of the ALS immunoreactivity from 25-µl aliquots of the samples (data not shown).
Nutritional and metabolic biomarker analyses. Serum glucose
concentrations (BioChem, Lakewood, NJ), free fatty acids (Wako Chemicals,
Richmond, VA), glycerol (Sigma Diagnostics, St. Louis, MO) and
-hydroxybutyrate (Sigma Diagnostics) were measured according to
manufacturer's instructions on an ATAC 8000 (Elan Diagnostics, Smithfield,
RI). Ferritin and transferrin were determined with solid-phase enzyme-linked
immunoabsorbent assays (Bethyl Laboratories, Montgomery, TX; American
Laboratory Products, Windham, NH). Prealbumin concentrations were determined
by using a nephelometric method (Minineph, The Binding Site, San Diego, CA).
The intra-assay variances were all <7%.
Statistical analyses. All data are presented as means ± SE.
A two (i.e., control vs. Exp) by three (i.e., days 1, 3, and
4) analysis of variance with repeated measures was employed for
statistical analyses for the study. Where appropriate, a Duncan's post hoc
follow-up test was used. A P value of 
0.05 was used for all
statistical tests. Pearson product moment correlations were calculated between
the changes in IGF-I measures and changes in nutritional and metabolic
biomarkers and body composition between days 1 and 4 of the
SusOps week. All statistical analyses were performed with Statistica software
packages (StatSoft, Tulsa, OK).
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RESULTS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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4,500 kcal/day. Body mass (control: 84.8 ±
3.7 kg; Exp: 82.2 ± 3.5 kg), fat free mass (control: 69.0 ± 2.7
kg; Exp: 67.7 ± 2.5 kg), fat mass (control: 15.8 ± 1.7 kg; Exp:
14.5 ± 1.8 kg), and %body fat (control: 18.4 ± 1.3; Exp: 17.4
± 1.5) all significantly declined (P < 0.05) during
Exp. IGF-I system responses. The temporal responses of the IGF-I system components are shown in Figs. 1 and 2. Most IGF-I system components were stable during the control week, with the exceptions being nonternary IGFBP-3 (decreased) and ALS (decreased). Total IGF-I, nonternary IGF-I, and free IGF-I are shown in Fig. 1. Compared with Exp day 1 concentrations, lower values were observed for total IGF-I (Exp day 1: 289 ± 36 ng/ml > Exp day 3: 197 ± 35 ng/ml = Exp day 4: 221 ± 29 ng/ml), nonternary IGF-I (Exp day 1: 25.6 ± 1.6 ng/ml > Exp day 3: 18.2 ± 1.5 ng/ml = Exp day 4: 18.7 ± 1.3 ng/ml), and free IGF-I (Exp day 1: 3.3 ± 0.5 ng/ml > Exp day 3: 1.7 ± 0.3 ng/ml = Exp day 4: 1.9 ± 0.3 ng/ml). Figure 2 shows the responses of the IGF system BPs. IGFBP-1 (Fig. 2A) increased (Exp day 1: 16 ± 6 ng/ml > Exp day 3: 110 ± 7 ng/ml = Exp day 4: 57 ± 14 ng/ml) during Exp. IGFBP-3 (Fig. 2B; Exp day 1: 3,769 ± 19.4 ng/ml > Exp day 3: 3,560 ± 25.2 ng/ml = Exp day 4: 3,547 ± 18.2 ng/ml) and nonternary IGFBP-3 (Fig. 2C; Exp day 1: 451 ± 19 ng/ml > Exp day 3: 392 ± 25 ng/ml = Exp day 4: 377 ± 18 ng/ml) both declined during Exp. Day effects, but not experimental effects, were observed for ALS (Fig. 2D; day 1 > day 3 = day 4).
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Table 2 illustrates the
proportion of IGF-I and IGFBP-3 existing as nonternary molecular complexes.
The proportion of IGF-I (11%) circulating in nonternary molecular
complexes was apparently not affected by the SusOps stress, whereas the
proportion of IGFBP-3 circulating in nonternary molecular complexes exhibited
a small but significant decrease (12.1 vs. 11.6%).
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Nutritional and metabolic biomarker responses.
Table 3 displays changes in
other measures of nutritional and metabolic biomarkers during the control
weeks and Exp. Ferritin, free fatty acids, glycerol, and
-hydroxybutyrate increased during SusOps, whereas transferrin was
unchanged and prealbumin decreased. Glucose concentrations were increased over
SusOps day 1 values on day 3 but not day 4.
Correlational analyses did not reveal any statistically significant
relationships between changes in any of the IGF-I system components with the
nutritional and metabolic markers or body composition variables.
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DISCUSSION |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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Our data indicate that the military operational stress scenario was
physiologically challenging, as evidenced by the estimated daily caloric
deficit (3,000 kcal), the loss in body mass (3.0%), and the limited
amount of sleep attained (total of 6.2 h). The 1.8% or 1.2-kg decline in
DXA-assessed lean mass should be interpreted with caution because of potential
artifacts introduced by short-term alterations in hydration status, although
they do suggest that the subjects were in a negative nitrogen balance. Total
IGF-I, nonternary IGF-I, free IGF-I, IGFBP-3, and nonternary IGFBP-3 all
declined during Exp, whereas IGFBP-1 increased and ALS was not altered.
Contrary to our original hypothesis, the reduction in IGF-I was proportionally
similar across all of the various molecular complexes (i.e., ternary vs.
nonternary), whereas the proportion of IGFBP-3 circulating in ternary
complexes exhibited a small but significant increase. This study demonstrates
that IGF-I system components differentially respond (both in direction and
magnitude) to the unique metabolic perturbation of this study. These
dissimilar alterations presumably influence IGF-I extravascular shifting,
half-life, and subsequent bioavailability.
IGF-I and IGFBP temporal responses. Total IGF-I concentrations
declined during SusOps and were 32 and 23% lower at 48 and 72 h, respectively.
IGF-I has been shown to decline by 67 and 70% after 5 and 10 days of complete
fasting in healthy adults (8,
15,
40) and by 50% after 14
days of military operational stress in Army Ranger students
(11). That nearly one-half the
magnitude of these reductions was achieved after only 48 h in the present
study underscores the severity of the caloric imbalance and metabolic strain
imposed by our SusOps model. Previous studies suggest that, during negative
energy balance, reductions in circulating IGF-I are a direct result of lowered
production from the liver (39,
40). These reductions occur
even in the presence of an amplification of growth hormone profiles and may be
influenced by other counterregulatory hormones (i.e., insulin and cortisol)
(19,
20). During a 10-day fast in
obese men, Clemmons et al. (8)
reported that IGF-I exhibited a linear and progressive fall, and Isley et al.
(15) reported that this fall
was accelerated during a similar fast in normal-weight subjects. These results
are in contrast to the present findings where the temporal response pattern
exhibited a marked decline after 48 h followed by a slight rebound over the
next 24 h. Using a rat model, Frystyk et al.
(13) also demonstrated that
the drop in IGF-I after 2 days of fasting had plateaued by day 3.
Thus the temporal response pattern for IGF-I for the present paradigm can be
best characterized as declining, then plateauing (i.e., nonlinear). One
possible explanation for this response could be the fact that our subjects
were ingesting daily calories and that the level of energy provided may have
been sufficient to support the maintenance of IGF-I concentrations after an
initial drop. Kupfer et al.
(23) reported that the levels
of energy and protein that support normal IGF-I concentrations are 20
kcal/kg body mass and 1 g protein · kg body
mass-1 · day-1,
respectively. Our subjects received 18.8 kcal/kg body mass and 0.80 g
protein · kg body mass-1 ·
day-1 (range = 0.6-1.1 g · kg body
mass-1 · day-1). However,
the protein content of the diet was lower preceding the day 3 blood
samples (see Table 1). It might
be possible that the acute changes in protein intake influenced the observed
responses of the IGF-I system from day 3 to day 4.
Of the BPs measured, IGFBP-1 and IGFBP-3 were most affected, with IGFBP-1
rising 250% and IGFBP-3 falling 6%. The striking increase in IGFBP-1 is
consistent with previous literature on fasting
(13,
16). IGFBP-1 is regulated by
insulin and cortisol, and is involved in glucose counterregulation
(1). IGFBP-1 is thought to
exhibit an inhibitory effect on IGF-I action by interfering with IGF-I
ligand-receptor interactions,
(18) and increases in IGFBP-1
and -2 are associated with decreases in free IGF-I
(3,
16,
26). Frystyk et al.
(13) have speculated that the
IGFBP-1 increase may be viewed as a protective mechanism by neutralizing the
insulin-like hypoglycemic activity of IGF-I and serving to mobilize energy
from fat and protein. Compared with total and free IGF-I and IGFBP-1 changes,
IGFBP-3 reductions were smaller in magnitude (5% decline from the control
week to Exp). Day effects were evident for ALS concentrations, although ALS
was seemingly unaffected by SusOps. ALS is also a component of the ternary
complex and has been shown to be reduced with fasting in many but not all
studies. The failure of the ALS to be influenced by the Exp was surprising and
suggests ALS responses lag behind IGF-I and IGFBP-3. The modest decline in
IGFBP-3 and the lack of change in the ALS ensure that IGF-I would remain
sequestered in the ternary complex and would restrain the insulin-like effects
of IGF-I on peripheral tissues
(24). It would appear from our
data that the ternary complex is a stable reservoir not easily disassembled,
even during short-term metabolic stress
(6). Our findings also help to
delineate a hierarchy with regard to the magnitude of reduction because IGF-I
> IGFBP-3 > ALS.
Nonternary IGF-I and IGFBP-3 temporal responses. The reduction in
IGF-I after 48-72 h of negative energy balance was proportionally similar
across all of the various IGF-I molecular complexes. Thissen et al.
(38) reported that, in
protein-restricted rats, the proportion of IGF-I in smaller molecular mass
complexes (30 kDa), as measured by size-exclusion HPLC, increased from
33% during control to 65% after protein restriction. Certain
pathophysiological conditions (i.e., growth hormone deficiency, starvation,
tumor hypoglycemia) have also shown that the ratio of IGF-I bound to the
ternary vs. binary complexes is decreased
(12,
16,
17). Furthermore, recent
studies (29,
35) have demonstrated that
both acute exercise and chronic physical training can increase circulating
concentrations of low molecular mass IGFBPs.
Conceptually, a caloric deficit might lead to a preferential binding of IGF-I in nonternary complexes due to a destabilization of the ternary complex (as evidenced by declines in either IGFBP-3 or ALS) and/or an increase in other smaller molecular mass BPs (i.e., BP-1 and -2). Redistribution of IGF-I from ternary complexes to lower molecular mass forms could facilitate IGF-I transport out of the vascular compartment and toward tissues (29, 40). The present study did not demonstrate that IGF-I was differentially partitioned among its various molecular forms during 3-4 days of underfeeding. Using protein malnutrition in a rat model, Oster et al. (33) also failed to observe any alterations in the ternary molecular complex. ALS is an integral component of the ternary complex, and because ALS is in 50-60% molar excess (1, 22), a precipitous decline may be necessary to significantly destabilize the ternary complex and alter IGF-I distribution between ternary and nonternary molecular complexes. ALS disassociation from the ternary complex may be the important regulatory step in shifting IGF-I from ternary to binary molecular complexes. It may also be that a more severe energy deficit (either in duration or magnitude) or a greater degree of protein restriction than the present study (as occurs in critical illness and other clinical conditions) is required before there is a decrease in the proportion of IGF-I circulating in ternary complexes.
A question that the present study could not address was whether the partitioning of IGF-I among the nonternary complexes was altered. There are six different BPs for IGF-I, and the magnetic separation procedures used in this study were not able to separate the relative concentrations of the BPs in the IGF-I binary pool. Because the IGFBPs are known to respond differentially to nutritional stress, it is possible that IGF-I was preferentially complexed with BPs that increase with fasting. The small but significant decrease in IGFBP-3 circulating in binary complexes and the increase in IGFBP-1 after SusOps might suggest that there was a shift in the distribution of IGF-I sequestered among the BPs.
Although it is difficult to ascertain the precise contributions for the singular effects of physical exertion, sleep deprivation, and energy restriction on the changes in the IGF-I system observed in this study, it is likely that the major influence was the energy deficit. Older et al. (32) have reported that 3 consecutive days of delta-wave sleep interruption had no effect on IGF-I, and acute physical exercise has either shown no change or increases in circulating IGF-I (29).
In summary, our results indicate that short-term military operational stress (i.e., caloric and sleep restriction superimposed on sustained physical exertion) lowers IGF-I and IGFBP-3, as well as nonternary IGF-I and nonternary IGFBP-3, and increases IGFBP-1. These alterations were concomitant with losses in body mass and lean mass but were not significantly correlated with changes in other traditional biomarkers of nutritional status. The decline in IGF-I was proportional among its various molecular complexes. In conclusion, during a short-term energy deficit associated with prolonged physical work and sleep disruption in young healthy men, 1) IGF-I system components differentially respond (both in direction and magnitude) and 2) the relative proportion of IGF-I sequestered in ternary vs. nonternary molecular complexes appears to be well maintained.
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DISCLOSURES |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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ACKNOWLEDGMENTS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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FOOTNOTES |
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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. Section 1734 solely to indicate this fact.
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REFERENCES |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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) and sustained operations (SusOps;
) weeks. Means ± SE are shown. With the exception of nonternary
IGF-I, all values were stable during the control week.
*Significantly different (P 