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Extreme Running Competition Decreases Blood Antioxidant Defense Capacity

Laboratoire de Physiologie et de Biomécanique de l’Exercice Musculaire, UFRAPS (G.M., C.G., F.R.-B., H.Z., S.V., A.G.-D.), FRANCE
G.I.S. sciences du Mouvement (G.M., C.G., F.R.-B., H.Z., S.V., J.C., A.G.-D.), FRANCE
Laboratoire de Biologie Cellulaire et Végétale, Faculté de Pharmacie, Université de Rennes (J.C.), FRANCE
Rennes Cedex, Département de Biologie Intégrée, CHUG, Grenoble (H.F.), FRANCE

Address reprint requests to: Guillaume Machefer, Laboratoire de Physiologie et de Biomécanique de l’Exercice Musculaire, UFRAPS Université de Rennes 2, EA 1274, Avenue Charles Tillon, Campus la Harpe, CS 24414, 35044 Rennes Cedex, FRANCE. E-mail: guillaume.machefer{at}uhb.fr

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 
Objective: We tested whether an extreme running competition ("Marathon of Sands") might alter the blood’s enzymatic and non-enzymatic antioxidant status in 6 well-trained athletes.

Methods: The Marathon of Sands is a competition consisting of six long duration races in the desert in which the athletes carry their own food. Blood samples were collected from an antecubital vein while the athletes were at rest before the competition and then again 72 hours after. Erythrocyte antioxidant enzyme activity (glutathione peroxidase, superoxide dismutase), erythrocyte glutathione level, plasma non-enzymatic status (vitamin C, alpha-tocopherol, retinol, ß-carotene and carotenoids) and plasma lipid peroxidation marker (TBARS) were measured.

Results: The Marathon of Sands induced a significant alteration of the blood antioxidant defense capacity. Indeed, 72 hours after the race, significant decreases were recorded in erythrocyte superoxide dismutase activity and in plasma concentrations of retinol, ß-carotene and other carotenoids. These changes were associated with a concomitant increase in erythrocyte glutathione and in plasma TBARS levels.

Conclusion: This study indicated that such extreme competition induced an imbalance between oxidant and antioxidant protection.

Key words: extreme competition, antioxidant vitamins, carotenoids, TBARS

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 
Numerous studies have demonstrated that long and strenuous aerobic exercise perturbs the physiological balance between oxidative products and the antioxidant defense system [1–3]. So, an exercise-induced oxidative stress may appear.

Exercise-induced oxidative stress may be intensified by high external temperature: in vitro and in vivo studies show a relationship between elevated temperature and increases in oxidative stress markers [4–7]. Moreover, various works indicate that low dietary intakes or deficiencies in antioxidant vitamins also promote oxidative stress [8–10].

The seven-day long "Marathon of Sands" is a self-dietary running competition organized under high temperature conditions in the Moroccan desert. It consists of six 24 to 84 km stages each day under average external temperatures of 25°C or more. During such strenuous exercise, adequate intake of antioxidant vitamins is essential [11] to protect the athletes against oxidative damage. However, athletes are asked to bring with them all the food they need for the week and to carry it on their back during the race. To limit the weight of the backpack, each runner tries to reduce his nutritional intake to an absolute minimum and uses pre-package food which is easy to conserve for many days in the heat. In these conditions, vitamin intake may be insufficient.

By associating repetition of long aerobic exercise, a restrictive diet and heat, this extreme competition may likely induce oxidant stress and alter the blood antioxidant system but it has never been demonstrated.

To clarify this hypothesis, the aim of the present report was to examine the changes of blood antioxidant defenses in these athletes upon their return to France, 72 hours after the end of the 2001 Marathon of Sands. Antioxidant protection was estimated by measuring erythrocyte superoxide dismutase (SOD) and glutathione peroxidase (GPx) activities, as well as erythrocyte reduced glutathione (GSH) levels. Moreover, we measured the concentrations of the main antioxidant vitamins in plasma: vitamin C, alpha-tocopherol and ß-carotene. We also analysed other plasma concentrations in antioxidant nutrients that are less studied in exercise-induced oxidant stress: retinol and the main human carotenoids. In order to estimate oxidant stress, we analyzed phospholipid membrane damage in plasma by measuring TBARS concentration.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 
Subjects
Data were collected on six healthy male long-distance runners undertaking regular running exercise who participated in the 2001 Marathon of Sands. They usually ran 84.0 ± 9.4 km per week and trained for ultradistance events for 13.2 ± 3.1 years. Their best marathon performance was 170.5 ± 9.0 min. All subjects were non-smokers and did not take any supplements including vitamins and medications. They gave informed consent prior to the beginning of the study.

Competition
In 2001, the Marathon of Sands competition consisted of 7 days of running divided into 6 races. During the first three races, subjects ran approximately 25, 34 and 38 km respectively. The distance of the fourth stage was 84 km. The race could have been finished on the fifth day depending on the physical ability of each subject. Stages 5 and 6 were both 42 km races. The races begun at 9 AM. During this competition, all athletes carried their own food and equipment which weighed between 5 and 15 kg at the beginning of the competition. The organization provided only the water, which was restricted to between 9 and 10.5 L per day according to the distance. As the precise composition of food (especially in antioxidant nutrients) did not appear on the pre-package food, it was impossible to evaluate the exact antioxidant intake. The temperatures during all the races were between 25 to 30°C.

Materials
Metaphosphoric acid (MPA), butylated hydroxytoluene (BHT), 1,1,3,3 tetramethoxypropane, phosphotungstic acid, thiobarbituric acid (TBA) and H₂SO₄ were purchased from SIGMA (St Quentin Fallavier, France). Acetic acid, ethanol and n-butanol were obtained from MERCK (Darmastadt, Germany). Vacutainers were purchased from Terumo Europe (Leuven, Belgium).

Experimental Procedure
Blood samples were collected between 9 and 10 AM from the antecubital vein at rest before the competition and 72 hours after its completion. Each time, the subject’s weight and body fat were recorded. Body fat percentage was estimated from 4 skinfold thicknesses according to the method described before [12]. On the first visit, a resting electrocardiogram was done followed by a maximal oxygen uptake (O_2max) test using a graded treadmill. Exercise was performed until exhaustion according to a method previously described [13]. An electrocardiogram was recorded throughout the test and O₂ was measured using a breath-by-breath automated exercise metabolic system (CPX, Medical Graphics, St. Paul, Minn., USA).

Blood Sample Preparation
Resting blood samples were collected using two different vacutainers. The first heparinized vacutainer was used to determine plasma TBARS, the erythrocyte GSH level, and erythrocyte SOD and GPx activities. Five hundred microliters of whole blood were stored at 4°C for one day before determining SOD activity and 150 µL of whole blood were frozen at –20°C for GPx activity determination (with a maximum conservation of 20 days). For GSH analysis, 500 µL of whole blood were centrifuged at 2500 g for 5 min at 4°C. The plasma supernatant was discarded and the erythrocyte pellets were suspended in 4 volumes of MPA (6% 1:1 in water). After shaking vigorously, it was centrifuged at 3000 g (10 min, 4°C). The aciditic protein-free supernatants were stored at –80°C until analysis. The rest of the blood samples were centrifuged (1500 g, 10 min, 4°C) and the plasma was used to determine TBARS (500 µL) the day of the experiment. The rest of plasma was aliquoted (1 mL for plasma alpha-tocopherol, retinol and carotenoids concentrations) and was stored at –80°C. For vitamin C determination, 500 µL of plasma were added to 4.5 mL of MPA (5% w/v) prior storage at –80°C.

The second vacutainer, containing EDTA, was used to determine hematocrit (Hct) and hemoglobin (Hb). Determinations of both Hct and Hb were realized in order to measure plasma volume changes [14], and determination of Hb was also realized in order to express erythrocyte enzyme activities per gram of Hb. For the assay of Hb, the vacutainer was analyzed with an automate (Gen’s Beckman Coulter, Margency, France). For the Hct measurements, whole blood was collected into micro hematocrit tubes, which were then centrifuged (Hema- C, Jouan, France) for 3 min. Hematocrit was recorded by measuring the ratio between the plasma volume and the total volume of the sample. Hematocrit measurements were done in triplicate. The rest of the blood samples were immediately centrifuged (1500 g, 10 min, 4°C).

Biochemical Analysis
The erythrocyte enzymatic system was evaluated by the measurement of erythrocyte GPx (EC 1.11.1.9) and SOD (1.15.1.1) activities. Both assays used a Randox test combination (Randox, Montpellier, France). The Ransel test was used for GPx activity. This method uses an enzyme-coupled reaction and measures the oxidation of NADPH by cumen hydroperoxide as substrate. The Ransod test for SOD activity determination employs xanthine and xanthine oxidase to generate superoxide radicals which react with 2-(4-iodophényl)-3-(4-nitrophenol)-5-phenyltetrazolium chloride (INT) to form a red formazan dye. SOD activity was then measured by the degree of inhibition of this reaction. All the results in enzymatic activities were expressed as U.g^–1 Hb.

Erythrocyte GSH was determined spectrophotometrically using the GSH-400 kit (Bioxytech, Oxis International, Portland OR) based on two steps. The first step leads to the formation of substitution products (thioethers) between a patented reagent (4-chloro-1-methyl-7-trifluromethyl-quinolinium methylsulfate) and all mercaptans present in the sample. The second step is a ß-elimination reaction that takes place under alkaline conditions. This reaction is mediated by a second reagent (30% NaOH) which specifically transforms the substitution product (thioether) obtained with GSH into a chromophoric thione whose maximal absorbance wavelength is at 400 nm.

Vitamins and Carotenoids
Plasma vitamin C concentration was determined by high performance liquid chromatography (HPLC) [15]. Alpha-tocopherol, retinol, - and ß-carotene, zeaxanthin, lutein, ß-cryptoxanthin and lycopene concentrations in plasma were measured using a reversed HPLC procedure [16].

Lipid Peroxidation
The plasma level of lipid peroxidation was estimated by the analysis of plasma thiobarbituric reactive substances (TBARS) using tetramethoxypropane as the standard. In order to prevent exogenous amplification of peroxidation by heating during the assay, TBARS were analyzed using a protocol previously described [17] which was adapted taking into account some recent recommendations [18].

Expression of the Results and Statistical Analysis
Repetitive exercise and heat exposure induce plasma volume changes (PV) which necessarily modify all measured plasma concentrations. Therefore, the plasma chemical values (antioxidant vitamins, carotenoids and TBARS) measured in this study were all corrected taking into account PV. PV was calculated using the equation which takes into account the Hct and Hb measured before and after the competition [14]. Moreover, as possible changes in erythrocyte number may occur following exercise, the antioxidant enzyme activities were expressed as U.g^–1 Hb.

The results are presented in absolute values in mean ± SEM. The Kolmogorov-Smirnov test for normality was used. Statistical comparisons between pre- and post-competition values were performed by a Student paired t test. A Pearson or Spearman test was used when normality of the data was passed or failed respectively to measure the relationship between two parameters. The limit of significance was set at p < 0.05.

	RESULTS

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Physiological Characteristics
Anthropometric characteristics of the subjects are given in Table 1. Mean O_2max measured during the graded treadmill test was 60.6 ± 3.8 ml. kg^–1 · min^–1. Average time needed to cover the total distance of the Marathon of Sands and mean speed during the competition were 36.2 ± 5.0 h and 7.4 ± 1.0 km · h^–1 respectively. The duration of each race was included between 2.0 ± 0.4 h (race 6) and 12.4 ± 1.2 h (race 4). The period of recovery between two different races was included between 19.1 ± 0.9 h (between race 5 and 6) and 35.6 ± 1.2 h (between race 4 and 5; the day 5 is a day of recovery). The weak variation of the SEM indicates that the recovery time of the group was homogenous.

Correlations
When pre- and post-race data of the 6 athletes were pooled, the plasma concentrations of retinol were positively correlated with the plasma zeaxanthin and -tocopherol concentrations. Similarly, the ß-carotene plasma concentrations were positively correlated with the -tocopherol plasma concentrations (Fig. 1).

View larger version (15K): [in this window] [in a new window]   Fig. 1. Relationships between the pooling pre- and post-race concentrations of the plasma concentration of retinol and zeaxanthin (A), retinol and -tocopherol (B) and between ß-carotene and -tocopherol (C).

	DISCUSSION

As indicated by their training habits and by their laboratory (O_2max) and field (running time during an usual marathon) performances recorded before the beginning of the Marathon of Sands, all the participants were well-trained endurance athletes. Despite the conditions, neither body mass nor fat was significantly affected by this extreme competition.

We could not exclude the possibility that the travel from Morocco may induce modification of the results (jet-lag, plasma volume variation induced either by dehydration with air conditioned or by fluid ingestion). To our knowledge, no study exists concerning travel-induced oxidant stress. Concerning the jet-lag, this factor could be excluded since there is no jet-lag between Morocco and France. Concerning plasma volume variation, our results took into account theses factors since data measured in plasma were corrected by plasma volume changes. So we assume that the travel did not induce significant changes of our results. But, even if changes occur during the travel (4h), they would be lesser than those resulting from one week of extreme endurance competition in the desert.

The Marathon of Sands significantly altered the enzymatic and non-enzymatic antioxidant system. Indeed, after 72 hours of recovery, the athletes exhibited a significant decrease in erythrocyte SOD activity while the GPx activity had not significantly changed. Whereas a rise in the SOD activity has been previously described after exercise-induced oxidant stress in human [19], a decrease was also observed either in in vitro [20] or in vivo oxidant stress [21–24]. Thus, there is not a "normal" time course of the recovery of SOD activity in response to exercise. The decrease in SOD activity is mainly explained by the inhibiting effect of an important production of H₂O₂, the substrate of the SOD [20]. In the present study, another hypothesis might be assumed, pointing to a deficiency in copper or zinc ions. Copper is essential in order to maintain the activity of the erythrocyte SOD (CuZn SOD) in the cytosol [25] and Zn serves as a cofactor for this enzyme. Firstly, studies provided evidence that Cu and Zn may be discharged by sweat [26,27], losses of which were obviously very large during the Marathon of Sands. Secondly, urinary losses of Zn could be greater during exercise [28] but it was not possible to realize this measurement in this work. Thirdly, a lack of sufficient intake seemed possible also since food containing Cu or Zn (liver and mainly seafood and shellfish) were lacking during the Marathon of Sands. The lack of change in GPx activity was in accordance with other previous studies using isolated exercise. No significant change was found in athletes after a long distance running or after a triathalon [1,29–30]. The repetition of long exercises during the Marathon of Sands seemed induced no other modifications than only one exercise in GPx activity.

Concerning the non-enzymatic antioxidant system, this study showed significant changes in the erythrocyte GSH concentration and in plasma concentrations of retinol, ß-carotene and of some carotenoids.

As it has been already found in humans during a three-day recovery period following 90 min of exercise at 65% O_2max [31], we found significantly higher values in GSH after the competition. Such a change is often described during oxidant stress and may reflect the production and release of GSH by organs such as the liver [32]. An inter-organ transport could then be established so as to help the muscles to react against the oxygen reactive species [33]. It is interesting to mention here that the post-competition increase in GSH values was inversely related to the concomitant decrease in SOD activity (r = –0.65; p < 0.05).

Before the Marathon of Sands, the plasma antioxidant vitamin status was in the usual range or slightly higher with reference to the previous values found in healthy populations of young and trained male adults for -tocopherol, vitamin C, retinol and ß-carotene [30, 34].

To our knowledge, no specific data are available nowadays concerning the normal plasma concentrations in carotenoids other than ß-carotene in highly trained males. However, the present values were either slightly higher [35, 36] or near these values [16] in the common population.

After their return, 4 of the 6 athletes showed a decrease in plasma -tocopherol and in vitamin C concentrations. For ß-carotene and all the other carotenoid except zeaxanthin, the whole group exhibited a significant decrease. As shown in Fig. 1, all of these changes were obviously interdependent. The relationship between retinol and zeaxanthin was understandable since zeaxanthin may be a precursor of retinol. By contrast, no direct chemical relationship exists between retinol and -tocopherol or between ß-carotene and -tocopherol. These findings suggested that the concomitant changes in these antioxidants were linked by the excessive production of reactive oxygen species which consumed such antioxidant agents.

These major results were in accordance with other human studies [3,30]. Previous work failed to observe significant changes in -tocopherol and vitamin C whereas plasma retinol concentration significantly decreased after an ultramarathon [3]. A decrease in plasma ß-carotene concentration was shown after a marathon race [30] and the same result was found after an exhaustive cycling exercise eliciting maximal oxygen uptake [37]. In the present study, the concomitant decrease of ß-carotene and of the other main carotenoids, well known to act as antioxidant agents [38], also indicated that carotenoids were probably required to protect the body. In vitro, the antioxidant effect of ß-carotene and of some carotenoids may be indirect via the regeneration of retinol or direct by scavenging several free radicals. The plasma decrease of these components strongly suggested that either the body’s retinol, ß-carotene and carotenoids stores and/or the nutrients intakes in these agents were not sufficient to maintain constant plasma levels.

Finally, the alteration in the blood enzymatic and non-enzymatic antioxidant status was associated with a significant increase in plasma TBARS content which argued in favor of a concomitant increase in MDA levels. In this study, we adapted the protocol [17] by adding the chain-breaking antioxidant butylated hydroxy toluene (BHT) in order to prevent the non-specific amplification of peroxidation during the assay [18]. An increase in TBARS was also described in several studies after a maximal oxygen uptake graded test [39], 30 min of running at 80% O_2max [40] or a half-marathon [19] and usually reflects a lipid peroxidation associated with oxidative damages.

	CONCLUSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 
The present study shows that extreme competition like the Marathon of Sands resulted in significant alteration of the blood enzymatic and non-enzymatic antioxidant systems. These results led to the recommendation that the athletes should obviously increase their daily antioxidant vitamin intakes during such competition.

	ACKNOWLEDGMENTS

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The authors thank Martine Chevanne, Dominique Paul, Marie-Thérèse Gougeon, Martine Godard and Michelle Jester for their technical assistance.

Received July 29, 2003. Accepted February 6, 2004.

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TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 

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