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Journal of Sports Sciences

ISSN: 0264-0414 (Print) 1466-447X (Online) Journal homepage: http://www.tandfonline.com/loi/rjsp20

Cellular immune activity in response to increased training of elite oarsmen prior to Olympic competition P.M. Jakeman , A. Weller & G. Warrington To cite this article: P.M. Jakeman , A. Weller & G. Warrington (1995) Cellular immune activity in response to increased training of elite oarsmen prior to Olympic competition, Journal of Sports Sciences, 13:3, 207-211, DOI: 10.1080/02640419508732229 To link to this article: http://dx.doi.org/10.1080/02640419508732229

Published online: 01 Feb 2008.

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Date: 08 December 2015, At: 09:52

Journal of Sports Sciences, 1995, 13, 207-211

Cellular immune activity in response to increased training of elite oarsmen prior to Olympic competition P.M. JAKEMAN, 1 * A. WELLER1 and G. WARRINGTON2 1

Applied Physiology Research Group, School of Sport and Exercise Sciences, University of Birmingham, Birmingham BIS 2TT and 2British Olympic Medical Centre, Northwick Park Hospital, Harrow, Middlesex HA1 3JU, UK

Downloaded by [University of Limerick], [Phil Jakeman] at 09:52 08 December 2015

Accepted 27 February 1995

This study investigated the changes in urinary neopterin, a biochemical marker of cellular immune activity, in elite male rowers undertaking a progressive increase in training prior to Olympic competition. Twenty-seven male rowers of the 1992 Great Britain team provided daily urine samples for a 4-week period of training that included 17 days of altitude training and 10 days of heat acclimatization. The mean (± S.D.) ratio of neopterin/ creatinine in urine increased from pre-training values of 135 ± 32 to a peak of 219± 121 μmol neopterin per mol creatinine on day 19 of training (P < 0.05). Changes in the ratio of neopterin/creatinine with training were found to be transient and highly variable between subjects, ranging from no change to peak values five-fold greater than baseline. On the basis of the in vivo measurement of cell-mediated immunity employed in this study, we conclude that elite athletes engaged in high-intensity training prior to competition show either no change or a moderate increase in cellular immune activation. Keywords: Cell-mediated immunity, exercise, neoptein, overtraining, rowing, training.

Introduction Elite athletes participating in intense training and competition are constantly challenging the limits of homeostasis and adaptation. With respect to the immune system, recent reviewers are of the opinion that moderate exercise may have a positive benefit upon immune function, whereas intense exercise, especially if performed repeatedly or for a long period of time, can impair adaptive immune reactions (Fitzgerald, 1988; Keast et al., 1988; Shephard et al, 1991; Cannon, 1993). The threshold for such an adverse immune reaction appears to depend upon the relative intensity of effort. In this respect, regular training may shift the threshold for an adverse reaction upwards, whereas unaccustomed or excessive training may shift the threshold downwards and make the athlete more vulnerable to infectious illness. However, opinion as to whether the immune system of the trained athlete is able to tolerate the stress of heavy

* Author to whom all correspondence should be addressed. 0264-0414/95

© 1995 E. & F.N. Spon

training remains equivocal (Smith and Weidermann, 1990; Verde et al., 1992). Changes in immunity following acute exercise or a period of training have been examined by immunological assays of lymphocyte function, which is believed to be the integral link between exercise and immunity. Intense, exhaustive exercise has been shown to induce a short-term (< 24 h) reduction in theT-cell helper/suppressor ratio, the natural killer (NK) cell response and immunoglobulin production; these changes in lymphocyte function are mediated, in part, by prostaglandin release from activated monocytes and neutrophils (Pedersen et al., 1990). Activated monocytes and macrophages also exert a pervasive influence on host defences by secreting cytokines such as interleukin-1 (IL-1) and tumour necrosis factor (TNF). These proteins act as molecular signals between immunocompetent cells and also induce a wide array of non-specific host defence adaptations known as the 'acute phase response'. Recent reports support the concept of a cytokine-mediated acute phase response during exercise (Sprenger et al., 1992) and provide a method of

Jakeman et al.

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investigating the adaptive responses of the immune reactivity to chronic exercise (training). The major limitation of this approach is the difficulty and expense of measuring circulating cytokine production and the limited time-window over which these measurements can be taken. In the present study, we measured changes in urinary neopterin, a biochemical marker of cell-mediated immunity, to monitor changes in the immune response of elite athletes prior to Olympic competition. Neopterin is synthesized and released by human monocytes/ macrophages after stimulation by interferon gamma and has been utilized clinically as a sensitive in vivo marker for the activation of the cellular immune system (for a review, see Wachter et al., 1992). In addition, an increase in circulating neopterin has been shown to be strongly correlated with a lowered CD4+/CD8+ T-cell ratio in patients with viral illness (Kern et al., 1984). A reduction in the T-cell helper/suppresser ratio is one of the most consistent findings related to exercise-induced immune suppression (see above). In the field of exercise immunology, Smith et al. (1992) have suggested the use of neopterin for use in the assessment of immune dysfunction in overtraining and/or chronic fatigue. Physical exercise induces several changes in cellmediated immunity, many of which are mediated via cytokine action (Pedersen, 1991; Sprenger et al., 1992). However, unlike the release of individual cytokines which can be short in duration and rapidly degraded in plasma, the measurement of neopterin is a more stable product of activated cell-mediated immunity and is readily detected in both plasma and urine. In a practical setting, urinary measurement offers the advantage of both convenience and reduction in the number of samples required to assess a response over a long period of time. There are no known cells that metabolize neopterin and the excretion of neopterin in urine conforms to a constant diurnal rhythm (Auzeby et al, 1988). In addition, the renal clearance of neopterin is greater than the standard value for the glomerular filtration rate (Werner et al., 1987), and therefore the neopterin/creatinine ratio measured in urine would not be expected to be influenced by changes in kidney function during exercise training. The measurement of the ratio of neopterin/creatinine in urine therefore provides a convenient and sensitive indicator of changes in cell-mediated immunity.

Materials and methods Subjects

Twenty-seven elite male rowers of the British Olympic team participated in this study. Their mean age and maximal oxygen uptake measured prior to the training

period were 26 (range 19-37) years and 5.92 (range 5.37-6.80) 1 min"1, respectively. Training programme

The subjects were monitored throughout a 4-week period of preparation prior to the Barcelona Olympic Games. All the subjects completed a 17-day period of training at altitude (2030 m; Silvretta, Austria) followed by a 10-day period of heat acclimatization (mean daily maximum ambient temperature 27°C; Varase, Italy). The following week, the athletes participated in Olympic competition. The average training time approximated to 3 h per day. Training intensity was assessed using the criteria defined by the Federation International des Societes d'Aviron (FISA) for rowingspecific and non-specific training. The non-specific training was primarily walking. Rowing-specific training is classified as being of low intensity (FISA categories I and II), medium intensity (category HI) and high intensity (category IV). Training intensity was generally lower in the early phase of altitude training, increasing in intensity after acclimatization to altitude and during the period of heat acclimatization (Fig. 1). Physiological measures

The measurement of maximal oxygen uptake (VO2 max) was performed prior to altitude training on a rowing ergometer (Concept II, Nottingham, UK) using a discontinuous incremental protocol. Oxygen uptake was measured using an on-line metabolic measurement system (Jaeger, UK). The VO2 m a x w a s established using the criteria recommended by the British Association of Sports Sciences: (1) plateau of less than 150 ml O2 min"1 per stage increase in workload; (2) RER greater than 1.10; and (3) blood lactate concentration greater than 10 HIM. Throughout the study, early morning resting heart rates and an inventory of general health and well-being were recorded by the team physician. Biochemical measures

First-pass morning urine samples were collected daily from all subjects. Aliqudts (2 ml) were decanted and stored frozen (—20°C in the dark) until analysis. Urine samples were analysed for neopterin and creatinine by reversedphase, high-performance liquid chromatography according to the method described by Wachter et al. (1992). Briefly, thawed urine samples were diluted (x 10) with EDTA (5 DIM) and aliquots (25 \il) injected onto an analytical column (125 x 4 mm, Spherisorb ODSII) and eluted with potassium phosphate (15 HIM, pH 6.4) at a flow rate of 0.8 ml min"1. Urinary creatinine was detected by absor-

Cellular immune activity during training of elite athletes



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walking high intensity medium intensity low intensity


2 3 4 5 6 7 8 9

10 1 1 1 2 13 14 15 16 17 18 19 2 0 2 1 2 2 2 3 2 4 2 5

Day bance at 235 nm and neopterin by its native fluorescence (Ex 353 nm, Em 438 nm). The inter-assay coefficient of variation for repeated analysis of 10 duplicated samples for neopterin and creatinine was 2.3 and 3.9%, respectively. Statistical treatment of the data

The data are presented as means (± S.D.) unless otherwise stated. The data were found to be normally distributed and were analysed by repeated-measures analysis of variance. Significance was accepted at the 0.05 level.

Results Physiological measures

The mean age and maximal oxygen uptake of the rowers was 26 (range 19-35) years and 5.92 (range 5.37-6.8) 1 min'1, respectively. Mean basal heart rate (49 ± 5 beats min"1) varied only minimally (± 2 beats min'1 day"1) and did not change significantly throughout the period of study. None of the subjects reported sickness, or exhibited symptoms of 'flu-like' or other illnesses. There were several minor training injuries, but none of these required the athlete to be absent from training for more than 1 day. Urinary neopterin, creatinine and neopterinlcreatinine ratio

The changes in the mean (« = 27) creatinine and neopterin concentrations and neopterin/creatinine ratio

Figure 1 Analysis of the training schedule of elite oarsmen (n = 27) for the 25-day period prior to Olympic competition.

measured in the first-pass morning urine samples over the 29 days of the study are presented in Fig. 2. The measured pre-training urinary neopterin/creatinine ratio (135 ± 32 umol neopterin per mol creatinine) was within the normal ranges for healthy subjects of similar age and sex (Wachter et al, 1992) and similar to previous studies on athletes (Weller and Jakeman, 1991): On ascent to altitude, there was a marked increase in urinary creatinine concentration of these urine samples, which normalized to pre-ascent levels on day 10. During this acclimatization phase, the concentration of neopterin in these samples remained stable, .then increased significantly above resting levels from day 12. The peak neopterin/creatinine ratio (219 ± 121 fimol neopterin per mol creatinine) was recorded 2 days after arrival at the heat acclimatization venue (i.e. after 19 days of training). Thereafter, the urinary neopterin/creatinine ratio declined to values that were not significantly different from those attained at the start of the study. Further analysis of the change in neopterin/creatinine data revealed a marked inter-individual variability in response. The majority of the subjects maintained near baseline ratios of neopterin/creatinine, while for eight of the subjects the ratio of neopterin/creatinine rose to peak values of between two- and five-fold basal levels.

Discussion For obvious reasons, there is a shortage of data on elite athletes undertaking prolonged periods of training and competition. 'Experimentation' with potential (and

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Jakeman et al.

actual) Olympic medallists is not easily controlled. Nevertheless, the nature of training for rowers (i.e. groups of subjects in one boat) is probably the closest that can be achieved in terms of experimental control in a practical setting. An important limitation to the study of immunology and training in the laboratory setting is that observations of cell-mediated proliferation and function are determined in vitro and are based on serial collection of specimens of peripheral blood. These data provide only a limited indication of the response in vivo. Using this approach in a previous study of elite cyclists forced to undertake an increased training load, we found that the resting plasma values of neopterin response to the superimposition of a maximal exercise test were not significantly elevated (Snyder et al, submitted). In the present study, we monitored the underlying trend in immune reactivity by measuring the ratio of neopterin/ creatinine in urine and observed an inter-subject variability of response to the exercise training regimen

1 3



9 11 13 15 17 19 21 23 25 27 29 DAYS

Figure 2 Changes in urinary neopterin and creatinine of elite oarsmen during training in preparation for Olympic competition. The data are presented as the mean ± S.D. (n = 27). *P

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