Elsevier

Pathophysiology

Volume 7, Issue 4, March 2001, Pages 263-270
Pathophysiology

Acute immune response in respect to exercise-induced oxidative stress

https://doi.org/10.1016/S0928-4680(00)00057-2Get rights and content

Abstract

The relationship between exhaustive exercise, oxidative stress, the protective capacity of the antioxidant defense system and cellular immune response has been determined. Exhaustive exercise in well-trained young men (n=19)-induced leukocytosis, decreased proportion of activated-lymphocyte subsets (CD4+ and CD8+) expressing CD69, decreased lymphocyte mitogenic response to concanavalin A (ConA) and phytohemagglutinin (PHA), increased lipid peroxidation, increased total antioxidant status (TAS) and catalase activity, immediately after exercise. Suppressed blood concentration of T-lymphocyte subsets (CD3+, CD4+, CD8+, NK), increased TAS and blood total glutathione (TGSH) in early recovery period (30 min after exercise) were found. Strong positive correlation was observed between TGSH and lymphocyte mitogenic response to ConA and PHA (r=0.85 and 0.85, respectively) immediately after exercise. Moderate positive correlation was observed between TAS and lymphocyte mitogenic response to PHA (r=0.59) immediately after exercise as well as between TAS and lymphocyte mitogenic response to PHA and ConA (r=0.69 and 0.54, respectively). Moderate to weak correlation was observed between TAS and conjugated dienes with exercise (r=0.66) as well as in 30-min recovery (r=0.50). After a short-term bout of exhaustive exercise, immune system was characterized by acute phase response, which was accompanied with oxidative stress. Suppression of the cellular immunity 30 min after exercise shows that this period is not enough for recovery after exhaustive exercise. The results suggest the interactions between exercise-induced oxidative stress and immune response.

Introduction

One of the most actual problems of sports medicine is to prevent athletes from disease and infections during intensive training and competition periods. The risk of infection near the decisive competition is significantly elevated, especially when, during training camps, the athletes live together and infection can be spread and ruin the work of several years. Although, moderate training enhances many aspects of immune function, exhaustive exercise may impair immune responses increasing athlete's susceptibility to infection [1], [2], [3], [4], [5], [6], [7], [8], [9], [10], [11], [12] and, possibly, to autoimmune diseases and cancer [13], [14]. Epidemiological data suggest that endurance athletes are at increased risk for upper respiratory tract infection (URTI) during periods of heavy training and up to 2-weeks period following competition [15]. Exercise-related immunological changes include signs of inflammation, such as release of cytokines, activation of immunocompetent cell lines, complement, and the induction of acute phase proteins [7], [8], [16], [17], [18], [19]. However, the signs of immunosuppression, such as decreased T and B cell function and impaired cytotoxic or phagocytic activity, can also be observed [20], [21], [22]. The immunological response to exercise comprises numerous alterations within the immune system; but how these processes are regulated is still largely unknown. There has been substantial evidence for link between the neurohormonal and the immune system [23], [24], [25]. It is thought that stress hormones like adrenaline and cortisol cause the mobilization of granulocytes from extracirculatory pool [26]. Plasma concentrations of adrenaline and noradrenaline increase almost linearly with the duration of exercise and exponentially with its intensity when expressed relative to individual maximal oxygen uptake [27], [28]. The expression of β-adrenoreceptors on T, B and NK cells, macrophages and neutrophiles provides the molecular basis for these cells to be targets for catecholamine signaling [29], [30]. On the other hand, it has been reported that catecholamines can autooxidize and lead to free radical production [31], [32] or undergo metal ion-catalyzed oxidation to free radical products [33]. Hence, they provide a potential source of free radical production during exercise.

Heavy exercise is associated with substantial increases in oxygen consumption and production of reactive oxygen species (ROS) [34], [35], [36], [37]. Strenuous exercise is known to induce oxidative stress [35], [37], [38], [39], [40], a state where pro-oxidants overwhelm the antioxidant defense capacity [41], [42], [43]. Previously, it has been shown that physical exercise may cause depletion and oxidation of GSH, a crucial factor in the maintenance of tissue-antioxidant defenses and in the regulation of redox sensitive-signal transduction [44], [45], [46], [47], [48]. Likewise, reactive oxygen species promote complement activation [49], as well as facilitate vascular translocation of leukocytes by inducing expression of adhesion molecules [50]. Despite the substantial evidence indicating that strenuous exercise induces oxidative stress and acute immune response, information concerning interactions between antioxidant defense and immune system within exercise is scanty. This study was, therefore, primarily focussed on monitoring of oxidative stress markers and cellular immune response within exercise until volitional exhaustion.

Increased knowledge about the cross talk between exercise-induced oxidative stress and acute immune response is important for developing means for maximizing the health benefits of exercise and improving sports performance.

Section snippets

Material and methods

Nineteen male endurance-trained athletes (age 22.21±5.58 years, VO2max 69.79±8.22 ml/kg/min) were recruited into the study after obtaining an informed consent. The experimental procedures and protocol conformed to the principles of the Declaration of Helsinki and were approved by the Human Ethics Committee of the University of Tartu. Reasons for exclusion included any deviation from the criteria of good health, smoking, chronic medication or vitamin supplementation.

Maximal oxygen consumption

The mean VO2max (69.72±8.73 ml/kg/min) indicated that the men were highly fit.

Hemoglobin and hematocrit

Both Hb concentration and Hct rose markedly with exercise (P=0.0004–0.0014), but returned to pre-exercise level in 30-min recovery period (Table 1).

Cellular immune response

Exercise until volitional exhaustion induced leukocytosis (P<0.00001) in the peripheral blood, which returned to pre-exercise level during 30-min recovery (Table 2). Neutrophilia was prominent (P<0.00001) immediately after exercise, but returned to pre-exercise level in

Discussion

Exercise until volitional exhaustion caused oxidative stress as evident from the lipid peroxidation data. Our finding of elevated serum TBARS and DC in post-exercise samples is consistent with previous reports [58], [59].

We found that serum total antioxidant status (ability to scavenge free radicals) increased significantly in 30-min recovery, which may indicate compensation in response to exhaustive exercise. Previously, it has been shown that half-marathon in 17 trained male runners induced

Acknowledgements

This work was supported by Estonian Science Foundation and Finnish Center for International Mobility.

References (71)

  • G.L. Ellman

    Tissue sulfhydryl groups

    Arch. Biochem. Biophys.

    (1959)
  • L. Goth

    A simple method for determination of serum catalase activity and revision of reference range

    Clin. Chim. Acta

    (1991)
  • M. Kretzschmar et al.

    Glutathione homeostasis and turnover in the totally hepatectomized rat: evidence for a high glutathione export capacity of extrahepatic tissues

    Exp. Toxicol. Pathol.

    (1992)
  • M. Mars et al.

    High intensity exercise: a cause of lymphocyte apoptosis?

    Biochem. Biophys. Res. Commun.

    (1998)
  • M.I. Hassan et al.

    Cis-platinum-induced immunosuppression: relationship to melatonin in human peripheral blood mononuclear cells

    Clin. Biochem.

    (1999)
  • R.W. Fry et al.

    Overtraining in athletes, an update

    Sports Med.

    (1991)
  • L. Hoffman-Goetz

    Influence of physical activity and exercise on innate immunity

    Nutr. Rev.

    (1998)
  • L.T. Mackinnon

    Immunity in athletes

    Int. J. Sports Med.

    (1997)
  • D.C. Nieman

    The immune response to prolonged cardiorespiratory exercise

    Am. J. Sports Med.

    (1996)
  • B.K. Pedersen et al.

    Immunity in athletes

    J. Sports Med. Phys. Fitness

    (1996)
  • D.B. Pyne et al.

    Effects of intensive exercise training on immunity in athletes

    Int. J. Sports Med.

    (1998)
  • P.N. Shek et al.

    Physical exercise as a human model of limited inflammatory response

    Can. J. Physiol. Pharmacol.

    (1998)
  • S. Shinkai et al.

    Acute exercise and immune function. Relationship between lymphocyte activity and changes in subset counts

    Int. J. Sports Med.

    (1992)
  • S.K. Singh

    Immuno-modulation by exercise: review

    Ind. J. Med. Sci.

    (1992)
  • M. Gleeson et al.

    The effect on immunity of long-term intensive training in elite swimmers

    Clin. Exp. Immunol.

    (1995)
  • T.B. Tomasi et al.

    Immune parameters in athletes before and after strenuous exercise

    J. Clin. Immunol.

    (1982)
  • S. Loft et al.

    Cancer risk and oxidative DNA damage in man

    J. Mol. Med.

    (1996)
  • B.K. Pedersen et al.

    Physical activity and cancer

    Ugeskr. Laeger.

    (1997)
  • D.C. Nieman

    Immune response to heavy exertion

    J. Appl. Physiol.

    (1997)
  • N. Tvede et al.

    The effect of light, moderate and severe bicycle exercise on lymphocyte subsets, natural and lymphokine activated killer cells, lymphocyte proliferative response and interleukin 2 production

    Int. J. Sports Med.

    (1993)
  • T.R. Samelman

    Heat shock protein expression is increased in cardiac and skeletal muscles of Fischer 344 rats after endurance training

    Exp. Physiol.

    (2000)
  • E. Fehrenbach et al.

    HSP expression in human leukocytes is modulated by endurance exercise

    Med. Sci. Sports Exerc.

    (2000)
  • B. Wolach et al.

    Aspects of leukocyte function and the complement system following aerobic exercise in young female gymnasts

    Scand. J. Med. Sci. Sports

    (1998)
  • H. Gabriel et al.

    Increased phagocytic capacity of the blood, but decreased phagocytic activity per individual circulating neutrophil after an ultradistance run

    Eur. J. Appl. Physiol.

    (1995)
  • D.C. Nieman et al.

    Indomethacin does not alter natural killer cell response to 2.5 h of running

    J. Appl. Physiol.

    (1995)
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