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Vol. 84, Issue 4, 1252-1259, April 1998
1 Departments of Health, Leisure, and Exercise Science and Biology, Appalachian State University, Boone, North Carolina 28608; 2 Immunology Center and Department of Pathology, Loma Linda University Medical Center, Loma Linda, California 92350; and 3 Department of Exercise Science, School of Public Health, University of South Carolina, Columbia, South Carolina 29208
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ABSTRACT |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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The influence of exercise mode and 6%
carbohydrate (C) vs. placebo (P) beverage ingestion on granulocyte and
monocyte phagocytosis and oxidative burst activity (GMPOB) after
prolonged and intensive exertion was measured in 10 triathletes. The
triathletes acted as their own controls and ran or cycled for 2.5 h at
~75% maximal O2 uptake,
ingesting C or P (4 total sessions, random order, with beverages
administered in double-blind fashion). During the 2.5-h exercise bouts,
C or P (4 ml/kg) was ingested every 15 min. Five blood samples were
collected (15 min before exercise, immediately after exercise, and 1.5, 3, and 6 h after exercise). The pattern of change over time for GMPOB
was significantly different between C and P conditions
(P 
0.05), with postexercise values
lower during the C trials. Little difference was measured between
running and cycling modes. C relative to P ingestion (but not exercise mode) was associated with higher plasma levels of glucose and insulin,
lower plasma levels of cortisol and growth hormone, and lower blood
neutrophil and monocyte cell counts. These data indicate that C vs. P
ingestion is associated with higher plasma glucose levels, an
attenuated cortisol response, and lower GMPOB.
immune system; cortisol; running; cycling; neutrophils; phagocytosis; oxidative burst
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INTRODUCTION |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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NEUTROPHILS AND MONOCYTES (55-65% and 3-9% of blood leukocytes, respectively) play an important role in nonspecific or innate immunity. These phagocytes act as the first line of defense to eliminate infectious agents and are involved in the muscle tissue inflammatory response to exercise-induced injury (23, 32, 37). The phagocytic response to infection and injury is complex and involves several stages, including adherence, chemotaxis, attachment, ingestion, and killing (23). The final killing stage involves the oxidative burst, which results in the production of cytotoxic reactive oxygen species (ROS), and degranulation, which involves the release of hydrolytic enzymes [e.g., elastase and myeloperoxidase (MPO)] and antimicrobial polypeptides from granules within the phagocyte (23, 32).
A growing number of studies have been conducted to define the response of phagocytic cells to prolonged and intensive cardiorespiratory exercise. Blood neutrophil and monocyte counts are elevated for several hours of recovery. Various mechanisms have been proposed, including exercise-induced changes in stress hormone and cytokine concentrations, body temperature changes, increases in blood flow, and dehydration (11, 18, 19, 22, 34). Most (2, 18, 21, 23, 24), but not all (9), studies indicate that heavy exertion increases the phagocytic activity of blood neutrophils and monocytes and stimulates the release of elastase and MPO (1, 3, 4, 7, 31). Less clear is the influence of heavy exertion on oxidative burst activity, with some studies indicating an increase (28, 30, 35) and some a decrease (8, 20, 21, 27) after exercise. Exercise duration and intensity and the method of detecting ROS appear to explain in part these mixed findings (32, 36). It has been proposed that exercise modes with a greater eccentric component (e.g., running vs. cycling) may cause ROS production to rise higher during the postexercise period because of increased muscle cell injury and inflammation (27, 32). However, experimental evidence measuring the influence of exercise mode on ROS production has not been published.
Although epinephrine, cortisol, and growth hormone have important effects on the trafficking of neutrophils and monocytes during and after exercise, there is uncertainty regarding the direct or indirect role of these stress hormones in their phagocytic and oxidative burst activity (23, 32, 35, 36). Suzuki et al. (36) showed that neutrophils mobilized from the marginated pool after heavy exertion have a higher potential of producing toxic oxidants through activation of the MPO pathway. These neutrophils may include band cells, which are recruited from the bone marrow, in part through the influence of cortisol, and appear capable of high ROS generation (34, 35). Thus intensive and prolonged exercise leading to a sustained elevation in cortisol may increase ROS generation to a greater extent than moderate exercise and low cortisol levels (28, 31-33).
Carbohydrate vs. placebo ingestion during prolonged endurance exercise has been associated with higher blood glucose and lower cortisol, growth hormone, and epinephrine responses, a diminished perturbation of blood leukocyte and lymphocyte subset counts, and a reduced inflammatory cytokine response (5, 12, 14, 16, 17, 21, 29, 31). Smith et al. (31) showed that carbohydrate ingestion attenuates the typical increase in plasma elastase concentration after 1 h of cycling.
Given the potential role of carbohydrate supplementation in affecting stress hormones and, therefore, the neutrophil and monocyte response to exercise and the impact that exercise mode may have on the inflammatory response and ROS generation, we designed a randomized, double-blind, placebo-controlled study to investigate the influence of supplemental carbohydrate on the immune response to 2.5 h of intensive running and cycling in triathletes.
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METHODS |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Subjects.
Ten experienced triathletes (8 men and 2 women) were recruited. They
met the following subject selection criteria: 25-50 yr of age,
marathon race time <4 h within the previous year, average training
distance 
30 km/wk running and 125 km/wk cycling during the previous
year, competition in at least two triathlon competitions, and ability
to run and cycle for 2.5 h within a laboratory setting. Triathletes
were chosen to ensure that all four running and cycling sessions could
be sustained at a high intensity for 2.5 h. Informed consent was
obtained from each subject, and the experimental procedures were in
accordance with the policy statements of the university's Institutional Review Board.
Experimental design.
The triathletes reported to the Human Performance Laboratory for
baseline measurements of maximal
O2 uptake
(
O2 max) and body
composition and to receive orientation regarding the study. Body
composition was assessed from hydrostatic weighing, and
O2 max was determined
twice using graded maximal treadmill and cycle ergometer protocols
(26). O2 uptake and ventilation
were measured using the CPX metabolic system (MedGraphics, St. Paul,
MN). Maximal heart rate was measured using the Q4000 stress test system
(Quinton Instrument, Seattle, WA). Training history and demographic
factors were assessed through a questionnaire.
O2 max
[verified by testing for O2
uptake, rating of perceived exertion (RPE) (26), and heart rate every
20 min]. Subjects exercised under carbohydrate (6% carbohydrate
beverage; Gatorade, Quaker Oats, Barrington, IL) or placebo conditions
(double blind). Sessions were assigned in random order.
Subjects recorded food intake for 3 days before each test session,
choosing foods from a list to ensure a carbohydrate intake of ~55%
of total energy intake. Nutrient intake was assessed using the
computerized dietary analysis system Food Processor Plus (version 6.0, ESHA Research, Salem, OR).
Test sessions.
For the four test sessions, subjects reported to the Human Performance
Laboratory in a 12-h fasted and rested condition at 0700. Subjects
indicated on surveys that they had avoided intensive exercise on the
day before testing and all exercise for at least 12-15 h, had
avoided mineral and vitamin supplements of >100% of the recommended
dietary allowance for 3 days before testing, and were free of symptoms
associated with respiratory infections. After the subjects rested for
10-15 min, a blood sample was taken. Next the triathletes consumed
12 ml/kg body mass of a 6% carbohydrate or placebo beverage. At 0730 the athletes began exercising and ingested 4 ml/kg carbohydrate or
placebo every 15 min of the 2.5-h exercise bout. The triathletes ran or
cycled from 0730 to 1000 at a pace adjusted to elicit a workload
approximating 75%
O2 max. Immediately
after exercise (at 1000), another blood sample was taken, followed by a
1.5-h recovery sample at 1130, a 3-h recovery sample at 1300, and a 6-h
recovery sample at 1600 (5 total samples). Subjects drank 8 ml · kg
1 · h1
carbohydrate or placebo during the first 1.5 h of recovery and then 4 ml · kg1 · h1
during the last 4.5 h of recovery. After the blood sample was taken at
1130, subjects ate a meal ad libitum, choosing foods from the same food
list to which they had adhered during the 3 days before the study. The
beverages were prepared by the Gatorade Sports Science Institute
(Barrington, IL). Treatments were double blinded, and carbohydrate and
placebo beverages were identical in appearance and taste. Except for
carbohydrate concentration, the two fluids were identical in sodium
(~19.0 meq/l) and potassium (~3.0 eq/l) concentration and pH
(~3.0).
Immune cell counts and assays. Five blood samples per subject were drawn from an antecubital vein with subjects in the seated position (after 10-15 min of rest, except for the immediate postrun sample). Routine complete blood counts with hemoglobin, hematocrit, and total leukocyte and subsets were performed by a clinical hematology laboratory (Lab Corp, Burlington, NC).
The phagocytosis assay utilized an FITC-labeled bacterium (Staphylococcus aureus; Molecular Probes, Eugene, OR) to quantify the degree of phagocytosis by granulocytes and monocytes, as described previously (21). Briefly, to determine the extent of oxidative burst exhibited by granulocytes and monocytes, we employed 2',7'-dichlorodihydrofluorescein diacetate (DCF-DA; Molecular Probes), a nonfluorescent molecule that is oxidized to green fluorescent dichlorofluorescein (DCF) as oxygen radicals are generated in the oxidative burst to kill unlabeled S. aureus. White blood cell count was determined using the Becton Dickinson Unopet manual counting protocol. Monocyte and granulocyte percentages were determined using two-color flow cytometric immunophenotying (CD45-FITC/CD13,14-PE). Bioparticle reagents of unlabeled and labeled S. aureus were suspended in PBS at a working concentration of 3 × 105 bioparticles/µl. After determination of the number of phagocytic cells in 100 µl of whole blood and addition of 15 FITC-labeled bacteria per cell, the mean channel fluorescence (FITC) was analyzed to determine the degree of engulfed bacteria (nonphagocytized bacteria were quenched with ethidium bromide; final concentration 200 µM). To determine the oxidative burst activities, DCF-DA (final concentration 100 µM; basal activity level) or DCF-DA and unlabeled bacteria (stimulated activity level) were added to 100 µl of whole blood. After the samples were incubated for 60 min (37°C) in the dark, the red blood cells were lysed, the samples were centrifuged, and the pellets were resuspended, the samples were acquired on the flow cytometer. For each sample, 1 × 104 phagocytes (monocytes and granulocytes) were acquired. Monocyte and granulocyte populations were analyzed individually for the extent of their phagocytosis and oxidative burst.Hormones, glucose, lactate, and plasma volume.
Five blood samples per trial per subject were drawn into heparinized
tubes and immediately chilled and centrifuged, with plasma samples
frozen at 
80°C until analysis for hormone and glucose levels. Glucose, insulin, cortisol, and growth hormone were measured from all blood samples. Catecholamines were anticipated to be near
baseline levels by 1.5 h after exercise and were not measured at 3 and
6 h after exercise. Plasma cortisol was assayed using a competitive
solid-phase 125I RIA technique
(Diagnostic Products, Los Angeles, CA) (21). RIA kits were also used to
determine plasma concentrations of insulin and growth hormone according
to the manufacturer's instructions (Diagnostic Products). For plasma
epinephrine and norepinephrine, blood samples were drawn into chilled
tubes containing EGTA and glutathione (RPN532 Vacutainer tubes,
Amersham) and centrifuged, and the plasma was stored at 80°C
until analysis. Plasma concentrations of epinephrine were determined by
HPLC with electrochemical detection (13, 21). Plasma was analyzed
spectrophotometrically for glucose (prerun and immediate and 1.5-h
postrun samples) (10). Blood samples were analyzed for lactate
according to the manufacturer's guidelines (Diagnostic Products).
Plasma volume changes were estimated using the method of Dill and
Costill (6).
Statistical analysis.
Values are means ± SE. Leukocyte subsets, hormone values, and all
immune function measures were analyzed using 2 (running and cycling
modes) × 2 (carbohydrate and placebo conditions) × 3 or 5 (times of measurement) repeated-measures ANOVA. If the condition × time or mode × time interaction was
P 0.05, the change from baseline
for the immediate postexercise and 1.5-, 3-, and 6-h recovery values
was compared between conditions or modes using paired
t-tests. For the four multiple
comparisons within conditions or modes, a Bonferroni adjustment was
made, with statistical significance set at
P < 0.013, and values between 0.013 and 0.05 were treated as trends.
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RESULTS |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Table 1 summarizes subject characteristics
for the 10 triathletes. Subject characteristics and test results of the
2 female subjects were within the range of the 8 male subjects, and
they fully complied with all aspects of the study design; thus results for all 10 subjects are presented without reference to gender. (The
percent body fat of the two female triathletes was 13.1 and 8.0%, and
their running O2 max
was 51.0 and 55.3 ml · kg1 · min1).
Although not an elite group, our athletes were highly experienced and
committed to triathlon training and competition, as demonstrated by the
data in Table 1. The maximal performance data indicate a 5% difference
between running and cycling for
O2 max, a
slightly lower maximal heart rate for cycling, and similar maximal
ventilation, respiratory exchange ratio, and respiratory rate for the
two modes.
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Nutrient analysis of the 3-day food records before each of the four test sessions revealed a consistent dietary intake: mean energy intake for the 10 triathletes ranged from 2,362 to 2,691 cal/day, with the proportion of energy as carbohydrate ranging from 54.6 to 57.5%, fat from 23.1 to 25.3%, and protein from 16.7 to 17.4%.
Percent O2 max, percent
maximal heart rate, respiratory rate, and ending lactate values did not
differ significantly among any of the four test sessions, indicating
similar relative workloads (Table 2).
Ending respiratory exchange ratios were significantly lower in the
placebo than in the carbohydrate conditions for both test modes. Ending
RPE values were lowest for the cycling-carbohydrate test session but
were similar for the other sessions (6-20 scale). The laboratory
temperature ranged from 24 to 30°C, with a relative humidity of
20-40% for all four test sessions. All triathletes consumed
fluids according to the research design, including 2.5 liters during
the 2.5-h run. Body mass remained stable pre- to postexercise (within
±0.6 kg of preexercise body mass for all test sessions). Plasma
volume changes were minimal and did not differ significantly among the
four test sessions (Table 2).
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The neutrophil, monocyte, and eosinophil data are summarized in Figs. 1-3. The pattern of change over time between test modes differed slightly for neutrophils (mode × time interaction, P = 0.02) and monocytes (P = 0.03); however, no pre- to postexercise changes differed significantly between running and cycling trials. For both modes the carbohydrate vs. placebo condition, however, resulted in significantly lower blood concentrations of neutrophils throughout recovery (condition × time interaction, P < 0.001). Immediately after exercise, blood monocyte counts were lower in the carbohydrate condition (P < 0.001). Blood eosinophil counts tended to be lower during recovery for the placebo conditions (condition × time interaction, P = 0.005) but were not affected by exercise mode (mode × time interaction, P = 0.131).
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Plasma glucose and insulin concentrations were higher in the carbohydrate than in the placebo conditions immediately after exercise but did not vary according to exercise mode (Table 3). The pattern of change in plasma cortisol was significantly different between placebo and carbohydrate conditions (but not modes), with values tending to be lower in the carbohydrate conditions during most of recovery (Table 3). The pattern of change in plasma growth hormone was significantly different between placebo and carbohydrate conditions (but not modes) and was highlighted by lower values in the carbohydrate conditions immediately after exercise (Table 3). The pattern of change in plasma catecholamines did not differ between placebo and carbohydrate conditions, although for norepinephrine, levels tended to be lower in the cycling test sessions (Table 3).
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Granulocyte and monocyte phagocytosis and oxidative burst activity data are depicted in Figs. 4 and 5. Granulocyte and monocyte phagocytosis (Fig. 4) increased after the exercise bouts, but the increase was attenuated in the carbohydrate trials (condition × time interactions, P = 0.05 and P = 0.01, respectively), with the largest contrasts between the carbohydrate-cycling and placebo-cycling trials. Exercise mode had a slight effect on granulocyte (mode × time interaction, P = 0.04) and monocyte (P = 0.12) phagocytosis, but no change was measured between pre- and postexercise values. The pattern of change over time for granulocyte (P = 0.04) and monocyte (P = 0.01) oxidative burst activity (Fig. 5) was significantly different between placebo and carbohydrate conditions, but not between running and cycling modes (P = 0.30 and P = 0.74, respectively), with the lowest 1.5-h postexercise values in the carbohydrate sessions.
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DISCUSSION |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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In this randomized, double-blind, placebo-controlled study, carbohydrate beverage ingestion significantly altered the pattern of change in plasma glucose, insulin, growth hormone, and cortisol; blood neutrophil and monocyte cell concentrations; and granulocyte/monocyte phagocytosis and oxidative burst activity after 2.5 h of intensive running and cycling. In general, exercise mode had no significant influence on these parameters.
Data from this study of triathletes and our previous study of marathoners (21) showed that 2.5 h of high-intensity exercise increase granulocyte and monocyte phagocytosis (of S. aureus bacteria) throughout 6 h of recovery. Most other studies have shown that heavy exertion increases the rate of phagocytosis by blood granulocytes (2, 23, 32), although neutrophil phagocytic activity in the upper respiratory tract area may be suppressed for extended periods of time after competitive running (15). Thus the clinical significance of our findings with blood phagocytes is unclear (25). The possibility exists that the increase in phagocytic rates by blood granulocytes after heavy exertion may reflect inflammatory processes and may have little relation to host protection against microbes (32).
Exercise mode, depending on the degree of eccentric muscle contraction (e.g., running vs. cycling) and subsequent inflammation, has been thought to influence granulocyte and monocyte functional responses (27, 32). Mode of exercise, however, had little effect on granulocyte and monocyte phagocytosis, but carbohydrate compared with placebo ingestion was associated with a reduction in peak values (pre- to 3-h postexercise increases were 40-48% for the carbohydrate trials vs. 64-84% for the placebo trials). Ortega (23) showed that cortisol enhances phagocytosis; thus it is likely that the lower phagocytic rates associated with carbohydrate ingestion in our triathletes were related to lower cortisol levels induced by higher plasma glucose concentrations (5, 16, 17).
In our previous study of marathon runners, oxidative burst activity (stimulated by the bacteria) fell 13.6% by 6 h of recovery for granulocytes but remained unchanged for monocytes, with carbohydrate ingestion having little effect on the overall pattern of change (21). Smith et al. (31) also reported that carbohydrate ingestion did not influence neutrophil oxidative burst activity after exercise, despite a reduction in plasma elastase concentrations. In the present study of triathletes, granulocyte and monocyte oxidative burst activity tended to rise slightly in the placebo running and cycling trials (7-18%) but remained the same or fell slightly in the carbohydrate trials (9-13%) by 1.5 h after exercise. These changes were small and reflect the degree of uncertainty in the literature. Although Smith and Pyne (32) advanced the idea that heavy exertion suppresses neutrophil oxidative burst activity, recent studies of athletes exercising intensively for >1.5 h suggest an increase during several hours of recovery (28, 30, 35, 36). Our data indicate that carbohydrate ingestion may attenuate the pattern of increase in granulocyte and monocyte oxidative burst activity after heavy exertion. Other factors that may influence oxidative burst activity are the time of blood sample collection and assay technique (36). We used S. aureus bacteria as the stimulating agent in our flow cytometric assay. Most other researchers utilized different types of stimulating agents (e.g., opsonized zymosan, phorbol 12-myristate 13-acetate, or N-formylmethionyl-leucyl-phenylalanine) with different assay techniques for ROS detection (e.g., luminol-dependent chemiluminescence, histochemical nitro blue tetrazolium, or ferricytochrome c reduction). Suzuki et al. (36) showed that these different methods have an effect on ROS detection but that, in general, exercise enhances ROS generation when the technique used measures activation through the MPO pathway. Thus intensive and prolonged exercise appears to cause an overall activation of neutrophil and monocyte function, with an increase in phagocytosis and generation of ROS (especially as a result of degranulation).
In summary, carbohydrate compared with placebo ingestion before, during, and after 2.5 h of intensive running and cycling by 10 triathletes who acted as their own controls had a significant effect in raising plasma glucose levels, decreasing plasma cortisol and growth hormone concentrations, and attenuating increases in blood neutrophils and monocytes. For 6 h after the running bout, an increase in blood granulocyte and monocyte phagocytosis was measured, with levels somewhat lower after the carbohydrate trials. Carbohydrate ingestion also diminished the increase in granulocyte and monocyte oxidative burst activity after exercise. Taken together, the data indicated that carbohydrate ingestion lessens hormonal and immune responses that have been related to stress and detrimental effects on various tissues through the indiscriminate action of ROS (36). Further research is warranted to determine the clinical significance of these findings on host protection against various pathogens.
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ACKNOWLEDGEMENTS |
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We acknowledge the assistance of Alex Koch, Elizabeth Shannonhouse, and Angie Ward.
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FOOTNOTES |
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This work was funded by The Gatorade Sports Science Institute (Quaker Oats, Barrington, IL).
Address for reprint requests: D. C. Nieman, Dept. of Health, Leisure, and Exercise Science, Appalachian State University, Boone, NC 28608.
Received 28 July 1997; accepted in final form 5 December 1997.
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Top
Abstract
Introduction
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Discussion
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