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Exercise Physiology Laboratory, Texas Christian University, Fort Worth, Texas 76129
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ABSTRACT |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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To determine the effect of carbohydrate (CHO) status on immune responses after long-duration exercise, on two occasions, 10 men completed a glycogen-depleting bout of cycle ergometry followed by 48 h of either a high-CHO diet (HiCHO; 8.0 g CHO/kg) or a low-CHO diet (LoCHO; 0.5 g CHO/kg). After the 48 h, subjects completed a 60-min ride at 75% maximal O2 uptake (EX). Blood samples were taken predepletion, pre-EX, post-EX, and 2 and 24 h post-EX and were assayed for leukocyte number and function, glucose, glutamine, and cortisol. The glucose responses were significantly higher in the HiCHO (4.62 ± 0.26 mM) vs. the LoCHO (3.19 ± 0.15 mM) condition post-EX, and glutamine was significantly higher in the HiCHO (0.472 ± 0.036 mM) vs. the LoCHO (0.410 ± 0.025 mM) condition throughout. Cortisol levels were significantly greater in the LoCHO (587 ± 50 nM) vs. the HiCHO (515 ± 62 nM) condition throughout the trial. Lymphocyte proliferation (phytohemagglutinin) was significantly depressed after exercise. However, there was no difference between conditions, and the depression was not correlated with elevations in cortisol. Circulating numbers of leukocytes, neutrophils, lymphocytes, and lymphocyte subsets were significantly greater in the LoCHO vs. the HiCHO condition at the post-EX and 2 h post-EX time points. These data indicate that the exercise and diet manipulation altered the number of circulating leukocytes but did not affect the decrease in lymphocyte proliferation that occurred after exercise.
blood glucose; glutamine; leukocytes; lymphocyte proliferation
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INTRODUCTION |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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ACUTE BOUTS of strenuous exercise have been shown to bring about alterations in the immune system, in the form of both depressed functional responses (9, 10, 29) and changes in the number of circulating leukocytes (9, 10, 29, 37). The altered immune responses resulting from exercise are short lived, and the clinical relevance is uncertain (14, 38). There may be a connection, however, between altered immune responses and the increase in the occurrence of infection that has been reported in some athletes during heavy training and after competition (2, 22, 25, 27, 32, 36).
The precise cause of the alterations in immune function has not been clearly identified. It is known, however, that heavy training and long-duration competitive events place considerable demands on the body's energy reserves. Depending on the dietary and exercise regimens of an individual, carbohydrate (CHO) stores can be acutely and/or chronically reduced (4, 19). Furthermore, plasma glutamine levels have been shown to undergo a reduction in response to heavy training (30), and they may be a metabolic marker for the overtraining syndrome (34). Because the cells of the immune system are highly dependent on blood glucose and glutamine as energy substrates (26, 31, 36), it is possible that the exercise-induced alterations in immune function are partially related to the levels of available substrates, such as glucose and glutamine, which can undergo significant decreases in response to specific dietary and/or exercise regimens (13, 19).
Furthermore, when the energy demands are high (for instance, in the case of prolonged exercise), the stress response is more pronounced, as evidenced by a concomitant elevation in counterregulatory hormones. Decreases in substrate availability produce elevations in cortisol, epinephrine, and growth hormone. Exercise alone also produces increases in these hormones; however, the combination of exercise and a pronounced counterregulatory response may have a more exaggerated effect on immune function.
Therefore, the purpose of this investigation was to determine the effect of preexercise carbohydrate status on immune cell numbers and lymphocyte proliferation before and after exercise. Specifically, the effects of high- and low-CHO diets (HiCHO and LoCHO, respectively) on lymphocyte proliferation and leukocyte counts were examined before and up to 24 h after 60 min of continuous submaximal exercise that was preceded by glycogen-depleting exercise and 48 h of dietary control (either 8.0 or 0.5 g CHO/kg body mass).
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METHODS |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Subjects.
Ten moderately trained men capable of completing 60 min of submaximal
cycle ergometry were selected as subjects. Each subject was initially
tested for maximal O2 uptake
(
O2 max) on an
ergometer by using a graded protocol. Results from this test were used
to establish the work loads for subsequent submaximal exercise tests. All subjects signed an institutionally approved informed consent form,
and they completed a medical history questionnaire to screen for major
contraindications to exercise testing. Subject characteristics are as
follows (means ± SE): age, 24.7 ± 4.8 yr; height, 179.0 ± 6.4 cm; body mass, 79.32 ± 7.45 kg; %fat, 10.17 ± 2.18; and O2 max,
3.93 ± 0.70 l/min.
Experimental design and protocol.
After the initial test for
O2 max,
each subject participated in two experimental trials administered in a
randomized, counterbalanced design with at least 2 wk between trials.
During the 24-h period before the experimental trial, subjects consumed
a standard mixed diet and did not engage in strenuous exercise. Each
experimental trial spanned 3 days, with testing performed at the same
time of day for each subject.
O2 max. During the
final 24 h, subjects remained inactive and consumed a self-selected,
normal mixed diet, which was duplicated for the two conditions.
Experimental testing.
The first blood sample was taken before the depletion ride and after 15 min of supine rest. The subjects were weighed, and then they completed
the 60-min depletion ride at 70% of
O2 max, followed by
six 1-min sprints, with 1 min of rest between each sprint. Respiratory
exchange measurements were taken by Douglas bag and analyzed on a
metabolic cart (Vista; Vacumed, Ventura, CA) during the 60-min ride to
verify exercise intensity. After the depletion ride, in the HiCHO
condition, they were given a prescribed diet of readily available
foods. The recommended food items were fruit, fruit juice, bagels,
bread, cola, and pasta with tomato sauce. In the LoCHO condition,
because of the difficulty in self-selecting a LoCHO diet, they were
given the actual food to be consumed for the next 48 h. This consisted
of cheese, eggs, bacon, tuna, and hamburger. Based on computer
analysis, the actual makeup of the HiCHO diet was 3,056 ± 277 kcal,
98.2 ± 24.2 g protein, 33.1 ± 10.3 g fat, and 604.4 ± 49.06 g CHO. The LoCHO diet consisted of 3,080 ± 302 kcal, 214 ± 9.6 g protein, 229 ± 34.2 g fat, and 34.0 ± 7.51 g
CHO. These diets corresponded to 7.62 and 0.43 g CHO/kg body mass for
the HiCHO and LoCHO conditions, respectively.
O2 max. In the HiCHO
condition, the subjects consumed a beverage that delivered 50 g CHO,
and in the LoCHO condition an equivalent amount of water was consumed.
This was done to further accentuate the differences in CHO status
between the two conditions. Respiratory exchange measurements were
taken by Douglas bag to verify exercise intensity and to determine the
rates of fat and CHO oxidation. CHO oxidation was calculated by using
the respiratory exchange ratio, liters of
O2 consumed, and standard tables
of caloric equivalency and percent contribution of fat and CHO.
Immediately after exercise, and at 2 and 24 h after the ride, blood
samples were taken after 15 min of supine rest. Subjects were allowed
to consume only water from the end of exercise until the blood sample
at 2 h.
Blood analysis. At each time point, blood was drawn from an antecubital vein into three different evacuated collection tubes (Vacutainer; Becton Dickinson, Mountain View, CA). The first contained heparin and was used for the lymphocyte proliferation measurements. The second contained EDTA and was used for the determination of leukocyte counts and lymphocyte subpopulations via flow cytometry. The third was a plain vacutainer to obtain serum for measurement of cortisol and blood glucose. Aliquots of whole blood were immediately removed from the latter tube and deproteinized in 8% perchloric acid to obtain an extract for the determination of lactate and glutamine.
Lymphocyte proliferation was conducted by using a whole blood method with the mitogen phytohemagglutinin (PHA; Difco Labs, Detroit, MI) (6). Briefly, after sampling, the blood was diluted 1:10 with glutamine-deficient RPMI 1640 (Sigma Chemical, St. Louis, MO) supplemented with either 0.0, 0.20, 0.50, or 2.0 mM glutamine. Two sets of triplicates of 100 µl of the diluted blood were then plated into microtiter plate wells for each level of glutamine (24 wells for each sample). PHA (100 µl) at a concentration of 100 mM was added to one set of the triplicate wells. The PHA also contained glutamine at concentrations of 0.0, 0.2, 0.5, and 2.0 mM to keep the final concentration of glutamine in the wells at the desired level. The second set of triplicate wells was used as a control and did not receive PHA. All samples were then incubated for 72 h in a humidified atmosphere of 5% CO2 at 37°C (model 8241; National Appliance, Portland, OR). After they were incubated, the cells were pulsed with 0.5 µCi tritiated thymidine (ICN Radiochemicals, Irvine, CA); 8 h later, the cells were harvested onto glass fiber filters with the use of a semiautomated cell harvester (model M12V; Brandel, Rockville, MD). Radiolabeled thymidine uptake was determined by using liquid scintillation counting (model LS 5801; Beckman Instruments, Irvine, CA). The flow cytometry procedure involved preparation of the cells by using a Coulter Immunoprep Leukocyte Preparation System (Q-Prep; Coulter Electronics, Hialeah, FL). A 100-µl aliquot of the cell preparation from the Q-Prep was washed with PBS and incubated at room temperature for 10 min with 5 µl of a monoclonal antibody for lymphocyte subsets and interleukin-2 (IL-2) receptor expression (Becton Dickinson). The monoclonal antibodies were conjugated with FITC, phycoerythrin (PE), and peridinin-chlorophyll-a-protein (PERCP) (Becton Dickinson). The conjugated monoclonal antibodies were specific for T lymphocytes [CD3+(PERCP)], helper/inducer lymphocytes [CD3+(PERCP)/CD4+(FITC)/CD8
(PE)], cytotoxic/suppressor lymphocytes [CD3+(PERCP)/CD8+(PE)/CD4(FITC)], B
lymphocytes [CD20+(PERCP)], natural killer cells
[CD16+(FITC)/CD56+(PE)], and IL-2 receptor expression
[CD25+(FITC)] on CD3+ cells. The antibody-labeled cells were analyzed by using a Cytoron Absolute flow cytometer (Ortho Diagnostics, Raritan, NJ). Complete and differential blood counts were
also determined from the blood drawn into EDTA-treated tubes by using
an automated analyzer (Sysmex K1000; TOA Electronics, Kobe,
Japan).
From the serum samples, blood glucose was determined by using a
colorimetric method (procedure 510; Sigma Chemical) on a
spectrophotometer (Spectronic 601; Spectronic Instruments, Rochester,
NY). Cortisol was determined by using an RIA method (procedure 2000-SP;
Diagnostic Systems Laboratories, Webster, TX) followed by detection of
counts per minute (cpm) on a Logic 111B gamma counter (Abbott
Laboratories, North Chicago, IL). Blood lactate was determined from
perchloric extracts by using the spectrophotometric enzymatic method
described by Lowry and Passonneau (20). Perchloric acid
extracts were also assayed for blood glutamine by using the
spectrophotometric enzymatic method described by Lund (21).
Statistical analysis. All data were analyzed using a two-factor ANOVA for repeated measures. The first factor (condition) had two levels, HiCHO and LoCHO. The second factor (time) had various levels, depending on the frequency of sampling (five levels for all of the variables based on blood samples). The dependent variables were body mass and CHO oxidation; blood glucose, lactate, and glutamine; leukocyte counts and lymphocyte subpopulations; and proliferation responses expressed as total cpm and cpm per lymphocyte subset. Differences detected by the ANOVAs were located with a Newman-Keuls post hoc test. Pearson correlations were run between various blood variables at specific time points. Significance was accepted at the P < 0.05 level.
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RESULTS |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Metabolic data.
The resting body mass in the HiCHO conditions did not change during the
48 h of dietary control (79.30 ± 2.51 vs. 79.39 ± 2.43 kg for
predepletion and preexercise, respectively). However, during this
period in the LoCHO condition, the subjects lost body mass (79.79 ± 2.30 vs. 78.94 ± 2.40 kg for predepletion and preexercise, respectively). The change in body mass for the HiCHO condition (0.08 ± 0.16 kg) was significantly less than in the LoCHO condition (0.85 ± 0.28 kg).
O2) responses (2.79 ± 0.12 and 2.85 ± 0.14 l/min for the HiCHO and LoCHO conditions,
respectively; Table 1). The average
exercise intensities relative to
O2 max were 71.17 ± 1.28 and 72.70 ± 0.77% for the HiCHO and LoCHO conditions,
respectively. The rates of CHO oxidation were significantly greater in
the HiCHO condition throughout the 60 min of exercise (Table 1).
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Proliferation data.
The proliferation responses from the cells incubated at 0.2, 0.5, and
2.0 mM glutamine were significantly higher than those in 0.0 mM
glutamine. However, there were no differences in the responses among
the three levels of glutamine (data for the predepletion time point
shown in Table 2). Because of the
similarity in the responses from the three levels of glutamine, the
responses from the cells incubated at 0.5 mM were used for the
statistical analyses. This level was chosen because it most closely
approximates physiological levels as determined by enzymatic methods
(39). The proliferation responses were expressed in three ways:
1) as total cpm of the stimulated
cells cpm of the control cells,
2) as cpm ( control) per
lymphocyte, and 3) as cpm ( control) per CD3+ cell. With the use of total cpm control (Fig. 5), there were
no differences between conditions. However, for both the HiCHO and
LoCHO conditions, the response at 2 h postexercise was significantly
lower than that at the predepletion time point. With the use of either
the cpm per lymphocyte (Fig. 6) or the cpm
per CD3+ cell (Fig. 7), there was again no
difference between conditions. The postexercise responses for cpm per
lymphocyte were lower than at all other time points, and the
postexercise values for cpm per CD3+ cell were lower than at all other
time points except the preexercise value. Correlations between cortisol
and proliferation responses expressed as cpm per lymphocyte and per
CD3+ cells were not significant (HiCHO,
r = 0.05 and 0.21; LoCHO,
r = 0.55 and 0.55 for cortisol vs. cpm
per lymphocytes and per CD3+ cells, respectively). Similarly, correlations between proliferation and blood glutamine levels were not
significant.
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Cytometric data. The number of leukocytes was significantly greater at the postexercise and 2-h postexercise time points in the LoCHO compared with the HiCHO condition (Table 3). A similar difference was observed in neutrophils, but it was only significant at the 2-h postexercise time point. The exercise-induced elevation produced a neutrophil percentage of 82% (vs. 54% predepletion) in the LoCHO condition compared with 68% (vs. 56% predepletion) in the HiCHO condition at the 2-h postexercise time point. Lymphocytes were different between conditions only at the postexercise time point. The elevation in neutrophil percentage at the 2-h postexercise time point corresponded to a reduction in lymphocyte percentage to 13% (vs. 36% predepletion) in the LoCHO condition and 23% (vs. 33% predepletion) in the HiCHO condition. Significant differences between specific time points within conditions for leukocyte, neutrophil, and lymphocyte numbers are noted in Table 3. In the LoCHO condition, the correlation (n = 10) between cortisol and leukocyte number at the postexercise time point approached significance (r = 0.627, P = 0.052), whereas that between cortisol and neutrophil number at the same time point reached significance (r = 0.762, P = 0.010). The corresponding correlations in the HiCHO condition were not significant (r = 0.417, P = 0.23; and r = 0.39, P = 0.265, respectively)
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DISCUSSION |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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The primary findings of this study were that the preexercise diet and exercise regimen, which was designed to produce a reduction in substrate availability in the LoCHO condition, did not bring about differences in exercise-induced decreases in lymphocyte proliferation compared with the HiCHO condition. There were, however, significant differences between conditions in the number of circulating leukocytes, neutrophils, lymphocytes, and lymphocyte subsets which may have been mediated by differences in hormonal responses that were present as a result of the dietary manipulation.
Metabolic responses. Preexercise CHO status can be assessed indirectly via such markers as changes in body mass and in blood glucose and lactate levels. The significant loss of mass during the 48-h period of dietary control in the LoCHO condition probably represents the loss of water that had been stored with liver and muscle glycogen. The significantly lower resting lactate levels and the tendency for a reduced resting blood glucose in the LoCHO condition are also suggestive of a reduced CHO availability.
During exercise, the significantly lower rates of CHO oxidation in the LoCHO condition and the lower postexercise blood glucose and lactate levels would be expected when CHO availability is reduced (4). The mean blood glucose of 3.25 mM at the end of exercise in the LoCHO condition was comparable to that typically associated with fatigue encountered at the end of endurance exercise (4). Collectively, the metabolic responses indicate that there was a lowered CHO status in the LoCHO condition.Proliferation responses. The lymphocyte proliferation responses followed a pattern of postexercise decreases that has been identified by previous researchers (8, 9). It was hypothesized that, after the 60 min of exercise in a CHO-depleted state, lymphocyte function would be impaired to a greater extent because of a reduced availability of substrate, i.e., glucose and/or glutamine. Although there were significant exercise-induced decreases in proliferation responses, there was no effect of the dietary manipulation, regardless of the method of determining the response.
The question of the degree of decline in blood glucose and/or glutamine that would elicit a depressed proliferative response has not been clearly identified. A methodological issue that should be kept in mind when analyzing these and other results is the tendency for lower plasma glutamine levels obtained with enzymatic methods (~0.5 mM) as opposed to those reported in studies using high-performance liquid chromatography and other methods (~1.0 mM) (23). Despite these methodological discrepancies, what is important in the present study is the relative differences between conditions. The influence of CHO status on the availability of glutamine and its concomitant effects on immune responses can be addressed from the standpoint of the influence of both diet and exercise. Greenhaff et al. (13) observed a significant decrease in resting plasma glutamine as a result of 4 days on a low-CHO (3% of total kcal) diet, whereas Blomstrand et al. (1) reported a significantly lower plasma glutamine with placebo compared with CHO ingestion, 5 min after 80 min of exercise. Others have reported significant decreases in glutamine in response to demanding exercise bouts, such as a marathon (18, 30), or after heavy training which elicited symptoms of the overtraining syndrome (23, 30). Although it is recognized that cells of the immune system use glutamine at relatively high rates (26), a diet or exercise-induced decrease in blood glutamine that leads to impaired cellular function has not been identified. It is difficult to conclude, therefore, that the decline of ~17% to mean values below 0.4 mM in the LoCHO condition represents a decrease that would impair lymphocyte proliferation. A comparable percent decline in plasma glutamine was, however, observed after a marathon (31) and in overtrained swimmers. However, in neither case was the decline directly linked to impaired immune function (23). Some investigators have shown that in vitro proliferation remains optimal with glutamine levels ranging from 0.3 to 1.0 mM (30, 31, 33). On the other hand, others report that the proliferative response is enhanced with increasing concentrations ranging from 0.1 to 1.0 mM, and that 0.5 mM is necessary for a complete transition through the cell cycle (17, 39). The similarity in the in vitro proliferation responses from cells incubated with 0.2, 0.5, and 2.0 mM glutamine in the current study supports the idea that glutamine levels below the normal physiological range may be adequate to support lymphocyte proliferation. Conversely, Moriguchi et al. (24) have demonstrated that glutamine supplementation in rats prevented exercise-induced decreases in both plasma glutamine levels and lymphocyte proliferation. These authors concluded that glutamine supplementation may have exerted its effects by directly affecting the responsiveness of lymphocytes to mitogens via an enhanced fuel availability. It has been suggested that exercise-induced changes in proliferative responses may be caused by the redistribution of cells rather than by actual alterations in the functional capacity of lymphocytes (10, 14). Frisina et al. (8) reported a decrease in mitogen-induced responses that was correlated (r = 0.78) with changes in T-cell number. Hinton et al. (14) reported similar relationships and also found that cultures of pure T lymphocytes did not show postexercise decreases in proliferation. When Nieman et al. (29) adjusted for the number of CD3+ cells in concanavalin A-stimulated whole blood samples taken before and after high- and moderate-intensity exercise, there was less depression of the mitotic response compared with the nonadjusted responses, particularly with moderate-intensity exercise. In the current investigation, the most noticable effect of using cpm divided by either lymphocyte number or CD3+ cells was that the depression of proliferation moved from 2 h postexercise to immediately after exercise. This shift can be attributed to the redistribution of circulating cells at the various time points. Thus, in the face of exercise-induced lymphocytosis, the proliferative response of the lymphocytes and, in particular, the T lymphocytes was reduced on a per-cell basis. These responses were obtained regardless of condition; thus these responses were not caused by dietary manipulation. The monoclonal antibody (CD25+) for the IL-2 receptor has been suggested as a more accurate means of assessing in vivo activation of lymphocytes than in vitro mitogen-stimulated proliferation (9). Previous investigators have reported mixed results regarding the effect of acute exercise on the number of CD25+ cells (9, 11, 35). The current results are difficult to interpret because of the lack of a significant interaction and the variable pattern of significant time effects. However, the significant main effect for condition suggests a tendency for a lower response cause by the LoCHO diet. Immunosuppressive effects of cortisol, particularly relative to lymphocyte proliferation, have been reported (40, 42). However, on the basis of previous findings from exercise studies, the relationship between elevated cortisol and decreased lymphocyte proliferation is not consistent (28, 29). In the present data, the temporal relationship between cortisol elevations and depressed lymphocyte proliferation (expressed per lymphocyte and CD3+ cell) suggests that a cortisol-induced suppression may have occurred; however, correlations between these two variables were not significant. Therefore, despite the significant condition main effect for cortisol, it is not possible to draw definitive conclusions regarding the effects of the glucose counterregulatory hormone responses on functional immune responses. An additional issue that should be considered is the potential influence of dietary fat on immune responses. In the LoCHO condition, >200 g of fat were consumed, which amounted to >60% of the caloric consumption. A high-fat diet can have inhibitory effects on the immune system, as shown by impaired lymphocyte proliferation and other functional responses (3, 25, 36). Although the majority of these effects have been produced with chronic consumption of a high-fat diet, potential effects of the 48 h of high-fat intake in the present study should not be overlooked.Cell number responses. The pattern of change in total leukocytes, neutrophils, lymphocytes, and lymphocyte subsets in both the HiCHO and LoCHO conditions is similar to that reported in previous investigations (11, 12, 16, 28, 29). Exercise has been shown to produce significant leukocytosis, neutrophilia, lymphocytosis, and elevations in lymphocyte subsets. The leukocytosis and neutrophilia may be sustained for a few hours of recovery; however, the lymphocytosis and elevations in lymphocyte subsets are typically followed by a significant depression during recovery (11, 29). It has been suggested that the changes in cell numbers are caused by the exercise-induced elevation in stress hormones and/or hemodynamic factors, both of which are intensity dependent (7, 11, 15, 29, 41). In the present investigation, the two bouts of exercise were identical in intensity. Thus, the greater cell number shifts in the LoCHO condition may have been caused by the hormonally induced indirect influence of differences in energy substrate availability. The presence of moderate correlations between cortisol and leukocyte and neutrophil numbers at the postexercise time point supports this conclusion. The clinical significance of the alterations in cell number in general, and the more exaggerated responses in the LoCHO condition, in particular, is uncertain.
In conclusion, although the diet and exercise regimen altered indicators of carbohydrate status during the 60 min of exercise, lymphocyte proliferation responses in the LoCHO condition were not different from those in the HiCHO condition. Thus, moderate differences in substrate availability did not explain exercise-induced changes in lymphocyte function. The significant differences between conditions in the number of circulating leukocytes, neutrophils, lymphocytes, and lymphocyte subsets which were observed may be explained by greater responses of stress hormones that were the result of the dietary manipulation. The clinical implications of the more pronounced numerical shifts in the LoCHO condition are not known. However, if possible, from a practical perspective, dietary CHO intake should be such that the more exaggerated responses are avoided.| |
ACKNOWLEDGEMENTS |
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This study was supported by the TCU Research and Creative Activities Fund.
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FOOTNOTES |
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Address for reprint requests: J. B. Mitchell, PO Box 297730, Texas Christian Univ., Fort Worth, TX 76129 (E-mail: J.Mitchell{at}TCU.EDU).
Received 16 June 1997; accepted in final form 9 March 1998.
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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, High-carbohydrate condition (HiCHO); 
,
low-carbohydrate condition (LoCHO); Pre-dep, predepletion; Pre-ex,
preexercise; Post and post-ex, postexercise. * LoCHO is
significantly different from HiCHO at designated time point.
a Significant difference
from predepletion and 24-h post-ex values within LoCHO condition. In
this and other figures, all significances are P < 0.05.
Main
effect for condition.
Significant main effect for
time, with postexercise value different from 2 h and 24 h postexercise
in both conditions.
