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Research Communication

Oxidative Stress in Humans during Work at Moderate Altitude^{1 ,2}

Wei-Hsun Chao, Eldon W. Askew³, Donald E. Roberts^*, Steven M. Wood and James B. Perkins^**

Division of Foods and Nutrition, University of Utah, Salt Lake City, UT 84112; ^* Department of Human Performance, Naval Health Research Center, San Diego, CA 92152; Medical Nutrition, Ross Products Division, Abbott Laboratories, Columbus, OH 43219; and ^** DataChem Laboratories, Incorporated, Salt Lake City, UT 84123

³To whom correspondence should be addressed.

	ABSTRACT

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Increased oxidative stress has been associated with work at high altitude; however, it is not known whether oxidative stress is a significant problem at moderate altitudes. The oxidative stress indicators, breath pentane (BP), 8-hydroxydeoxyguanosine (8-OHdG), oxygen radical absorption capacity (ORAC), 4-hydroxynonenal (4-HNE), malondialdehyde (MDA), and lipid peroxides (LPO) were measured in breath, blood and urine samples of U.S. Marines engaged in moderate altitude (~3000 m) cold weather field training. The test subjects were divided into a placebo and four antioxidant supplement groups (n = 15/group) and received the following supplements for 28 d: 1) vitamin E, 440 -tocopherol equivalents (-TE); 2) vitamin A, 2000 retinol equivalents (RE) of ß-carotene; 3) vitamin C, 500 mg ascorbic acid; 4) a mixture of 440 -TE, 2000 RE of ß-carotene, 500 mg ascorbic acid, 100 µg selenium and 30 mg zinc daily. Strenuous work (~23 MJ/d) in cold weather at moderate altitude was accompanied by increases in several indicators of oxidative stress that were not effectively controlled by conventional antioxidant supplements. The group receiving the antioxidant mixture exhibited lower BP (P < 0.05) compared with those receiving single antioxidant supplements; however, not all markers of oxidative stress responded like BP. Because these markers did not respond in the same manner, it is important to include markers from more than one source to assess the effect of supplemental dietary antioxidants.

KEY WORDS: • oxidative stress • indicators of oxidative stress • antioxidants • breath pentane • exercise • altitude • cold • military rations • humans

	INTRODUCTION

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When the body's natural defense systems against free radicals are overwhelmed by the excess formation of reactive oxygen species such as superoxide (O₂^-·), hydrogen peroxide (H₂O₂) and the hydroxyl radical (OH^·), oxidative stress increases. Reactive oxygen species are generated continually as by-products of aerobic metabolism, UV light exposure, hypoxia, pollution and other stresses (Jenkins and Goldfarb 1993 ). Oxidative stress may increase during strenuous physical activity, due to a 10- to 15-fold increase in oxygen consumption to meet energy demands, coupled with a small amount (1–2%) of "electron leakage" from the electron transport chain with subsequent direct reduction of molecular oxygen to the superoxide anion (Alessio 1993 , Clarkson 1995 , Kanter 1994 , Witt et al. 1992 ).

Oxidative stress can damage cellular membranes, cause cellular swelling, decrease cell membrane fluidity, prevent maintenance of ionic gradients and lead to tissue inflammation, DNA damage and protein changes, which can result in fatigue, delayed onset muscle soreness and increased injury recovery times (Alessio 1993 , Davies et al. 1982 , Halliwell et al. 1992 , Pyne 1994 , Seward et al. 1995 ). During work at high altitude, oxidative stress may be even greater than at sea level due to a combination of factors, i.e., temperature fluctuations, poor blood oxygenation due to hypoxia and resultant localized anoxia/reoxygenation with intermittent exercise, increased intensity of UV light and increased metabolic rate (Askew 1995 , Gossum et al. 1988 , Simon-Schnass 1996 ). Erythrocyte peroxidation and breath pentane (BP)⁴ production increase at high altitude (5100 m) and may be reduced by vitamin E supplementation (Simon-Schnass 1996 ). Similar studies have not been reported for lower elevations (~3000 m) at which many people live and recreate.

The cellular antioxidant defense system of the body may be expanded by dietary supplementation of antioxidant vitamins and minerals under conditions of elevated oxidative stress. Supplementation may reduce oxidative stress, decrease short-term tissue damage and long-term health risks associated with oxidative stress (Jacob and Burri 1996 ). Supplementation may be warranted when the diet is known to be poor in antioxidant nutrients or when the level of oxidative stress surpasses the body's antioxidant defense system capacity in individuals consuming an otherwise "adequate" diet.

We studied U.S. Marine Corps volunteers participating in strenuous winter field training at moderate altitude as a test model to examine markers of oxidative stress in breath, blood and urine and to evaluate the effectiveness of several antioxidant nutrient supplements. The purpose of this study was to determine whether extended periods of strenuous work in a multistressor environment increased oxidative stress and, if so, which antioxidant supplement or combination of supplements would be most effective in controlling or preventing these potentially damaging reactions.

	SUBJECTS AND METHODS

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Subjects and research design.

A randomized double-blind study was conducted with 75 male volunteers (mean age 24.4 ± 6.4 y) from the United States Marine Corps, Camp Pendleton, CA, undergoing winter field training at the Marine Corps Mountain Warfare Training Center in the Sierra Mountains northwest of Bridgeport, CA. This study was conducted under an approved human use protocol from the Naval Health Research Center, San Diego and adhered to NAVHLTHRSCHCEN Inst 6500.2, concerning the protection of human volunteers in medical research. The Marines camped at altitudes ranging from 2546 to 2804 m above sea level. Events and daily activities often took place at altitudes >3048 m. Activities included military skiing, mountain warfare tactics, mountain patrolling, snowshoeing, bivouac routine, survival skills, avalanche avoidance, rescue and mountain navigation. Test subjects were assigned randomly to one of the following four antioxidant treatment groups or a placebo group (n = 15/group): 1) vitamin E, 440 -tocopherol equivalents (-TE; unspecified isomer forms); 2) vitamin A, 2000 retinol equivalents (RE) of ß-carotene; 3) vitamin C, 500 mg ascorbic acid; 4) mixture of 440 -TE, 2000 RE of ß-carotene, 500 mg ascorbic acid, 100 µg selenium and 30 mg zinc; and 5) placebo control group, 1000 mg oyster shell calcium (CaCO₃) daily for 28 d (supplements purchased from Thrifty Payless, Wilsonville, OR). Supplements were started 14 d before the field study and continued for the 14 d of the study; the daily dose was given half in the morning and half with the evening meal.

Data collection periods.

Data were collected at three time periods. Period 1: on d 0 (at base camp immediately before field training), breath, blood and urine samples were collected. Nude weights of subjects were measured by an electroscale. Skinfold thickness was measured (Harpenden Caliper; Holland, MI) at the chest, abdomen and thigh on each subject in two consecutive sets; the measurements were averaged and used to calculate percentage of body fat. Period 2: on d 6 (during field training), breath and urine samples were collected. Food records (3-d) were obtained during this time period. Period 3: on d 14 (immediately after the end of field training), breath, blood and urine samples were collected. Final body weight and skinfold data were also obtained as described for d 0.

Diet.

Food (military rations) consumed during field training were as follows: 1) Meals, Ready to Eat (MRE); 2) Ration, Cold Weather (RCW); or 3) hot meals prepared at the base camp kitchen and delivered to the field. Four MRE provided 21.8 MJ/d (5200 kcal/d), whereas one RCW provided 18.8 MJ/d (4500 kcal/d). Three-day food records were analyzed (Nutritionist IV; First Data Bank, San Bruno, CA) to estimate energy consumption. Energy consumption projected from the 3-d food records coupled with an estimate of the energy equivalent of the change in body weight was used to estimate energy expenditure during the 14 d of field training.

Breath analyses.

Breath samples were obtained from each volunteer using a collection apparatus, collecting ~1000 mL of the subsequent deep alveolar exhalation in a tedlar bag (Norton Performance Plastics, Akron, OH). The alveolar air sample (300 mL) was then analyzed for pentane [a 5-carbon end product of the peroxidation of (n-6) fatty acids] by DataChem Laboratories, Salt Lake City, UT, by cryotrap/gas chromatography (Hewlett-Packard 5890 gas chromatograph, Palo Alto, CA) with flame ionization detection (column, Chrompack PLOT-U 25m x 0.32 mm i.d.; detector, flame ionization detection at 220°C; air, 250 kPa; hydrogen, 110 kPa).

Blood analyses.

Plasma was separated in heparinized tubes after centrifugation at 1000–1500 x g for 10 min, frozen on dry ice and shipped to Ross Products Division, Abbott Laboratories, Columbus, OH for plasma total lipid peroxide (LPO) analysis using a commercial kit from Kamiya Biochemical (Thousand Oaks, CA) (Ohishi et al. 1985 ).

A second tube of blood (no anticoagulant) was collected, and serum was obtained after clotting and centrifugation at 1000–1500 x g for 10 min. Samples were immediately frozen on dry ice and shipped to Genox, Baltimore, MD, for the following analyses: 1) serum -tocopherol, ascorbic acid and ß-carotene were measured by HPLC on a Hewlett-Packard 1090 HPLC system (Stacewicz-Sapuntakis et al. 1987 ). Ascorbic acid was analyzed by a colorimetric procedure using the disodium salt of ferrozine (McGown et al. 1982 ); 2) total aldehydes malondialdehyde (MDA) + 4-hydroxynonenal (4-HNE) were measured using a lipid peroxidation assay kit (Calbiochem, San Diego, CA) (Esterbauer and Cheeseman 1990 ); 3) serum total oxygen radical absorption capacity (ORAC), which measures the total antioxidant capacity of the serum, was determined by fluorescence of the oxidized ß-phycoerythrin indicator protein (Cao et al. 1993 , Delang and Glazer 1989 ).

Urine analyses.

A midstream urine sample (50 mL) from the first morning void was collected. Urine samples were analyzed for specific gravity, frozen, before the following analyses: 1) urine total aldehydes were measured as described previously for serum total aldehydes; 2) urine MDA was detected by a colorimetric assay using 2,4-DNPH reagent after separation by HPLC at 305 nm (DataChem Laboratories, Salt Lake City, UT); 3) urine 8-hydroxydeoxyguanosine (8-OHdG) was determined using a monoclonal antibody-based ELISA kit (Genox, Baltimore, MD) (Shigenga and Ames 1991 ).

Statistical analysis.

Statistical analyses were performed using SPSS (SPSS, Chicago, IL). Comparisons of change-from-baseline or "change scores" (d 0 value–d 14 value) between treatment groups (treatment vs. placebo) were performed using independent groups separate variance Student's t tests (Snedecor and Cochran 1980 ). The number of multiple comparisons was restricted by comparing each treatment group only with the placebo group because the purpose of the study was to determine whether individual antioxidants would reduce oxidative stress compared with the placebo. Paired t tests were performed to evaluate changes in oxidative stress within groups from d 0 to 14. To evaluate the overall cumulative oxidative stress when treatment effects were not significant, the five treatment groups were combined into one group and collectively analyzed (d 0 vs. 14) for indicators of oxidative stress. The Pearson correlation coefficient was used to test the relationships among the various indicators. All P-values were for two-tailed tests (P < 0.05) and represented as means ± SD

	RESULTS

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Body composition and nutrient intakes.

Subjects lost an average of 3.4 kg body weight and 1.8% body fat during the 2-wk training period (data not shown). There were no significant differences among treatment groups for body weight or body fat change. Energy distribution of the weight loss was ~41% from the fat-free mass and 59% from the fat mass. Euhydration was confirmed by noting equivalent urine specific gravities on d 0 and 14 (data not shown). Energy expenditure, energy intake, percentage of energy derived from macronutrients and dietary intake (exclusive of supplements) of vitamins E, A, C, iron and zinc were similar among treatment groups (Table 1 ). The mean daily energy expenditure during 2 wk of field training was ~23 MJ (5500 kcal) as estimated by the intake-balance method.

An increase in BP excretion during training was observed in all groups (Table 2 ), although only the vitamin E, A and placebo groups achieved significance, (P < 0.05). The change in BP excretion from d 0 to 14 was significantly reduced (P < 0.05) only for the antioxidant mixture group compared with the placebo group. After 14 d of training, oxidative stress, as reflected by plasma LPO, increased significantly (P < 0.05) (Table 3 ). Serum total aldehydes did not change significantly (data not shown), except in the vitamin C group (d 0, 2.74 ± 0.36 vs. d 14, 3.00 ± 0.41 µmol/L, P < 0.05). Serum ORAC values did not change significantly during the course of the study (data not shown). The oxidative stress indicators for urine (MDA, total aldehydes and 8-OHdG) tended to increase in all groups during training but there were no significant antioxidant treatment effects (data not shown). Because there were no significant treatment effects, test subject data were pooled to examine the increases in urine oxidative stress indicators (Table 4 ).

	DISCUSSION

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This study expanded the results of a preliminary study (Pfeiffer et al. 1999 ) by including more indicators of oxidative stress and antioxidant supplements administered individually and in combination. Oxidative stress increased in all groups in this study after 2 wk of strenuous field training work as evidenced by elevated BP (Table 2) , serum LPO (Table 3) and urine MDA, total aldehydes and 8-OHdG (Table 4) . The increase in 8-OHdG excretion in the urine observed in this study indicates either increased oxidative DNA damage or possibly increased repair of the damage (Halliwell 1999 ). The data agree with those of Okamura et al. (1997) who found that repeated exercise augments oxidative stress and DNA damage. Loft et al. (1994) proposed that oxidative DNA damage correlates with the rate of oxygen consumption in humans. The oxidative stress observed in this study might be due in large part to the high rates of energy expenditure (~23 MJ/d) of these Marines during field training.

The BP portion of this study agrees with earlier measures of BP excretion at higher altitude (5100 m) by Simon-Schnass (1992 and 1996) and Simon-Schnass and Pabst (1988) . Our study demonstrated that an increase in BP excretion also occurs during work at modest elevations (~3000 m). The antioxidant mixture supplement treatment significantly reduced BP at d 14 compared with the placebo group (P < 0.05). The lack of a significant vitamin E effect at moderate altitude in our study contrasts with a more pronounced effect of a vitamin E supplement on BP excretion noted by Simon-Schnass and Pabst (1988) at higher altitude. It is possible that individual antioxidants such as vitamin E may exert a more significant protective effect under conditions of greater oxidative stress.

The lack of a greater supplemental antioxidant effect in this study might be attributable to the customary fortification of military field rations with relatively high of dietary antioxidants (~150% higher in vitamin E, 400% higher in vitamin A and 700% higher in vitamin C compared with the Recommended Dietary Allowance). These Marines were also highly physically trained; they may have already developed an efficient antioxidant enzyme defense that (together with diet) may have achieved significant protection against oxidative stress. This explanation also agrees with our observation that serum ORAC was not enhanced by the antioxidant treatments. Halliwell (1999) noted that an intervention with a supplement may show an effect in a "poorly nourished" group, but not in a "well-nourished "group. It is also possible that indicators such as BP may reflect primarily immediate or short-term oxidative stress; other indices in blood or urine may reflect accumulated or longer-term oxidative stress. BP did not correspond closely with urine and blood indicators of oxidative stress. Hence, the timing of the collection of breath pentane may be important to its interpretation and utility as an indicator of overall oxidative stress (sampling several times during the day may be required).

Overall, five indices of oxidative stress (BP, serum LPO, urine MDA, total aldehydes and 8-OHdG) significantly increased (d 0 vs. 14, P < 0.05), whereas serum total aldehydes and ORAC did not.

The information from the antioxidant supplementation treatments under the conditions of this study was somewhat inconclusive, perhaps due to the large individual variations observed in the subjects. Individual differences existed in the amount of exercise or work accomplished daily, degree of prior physical training, sunlight exposure, prior dietary habits, individual variation in selection of food items or smoking; all of these could contribute to within-test subject variability. The results of this study did not clearly indicate that the vitamin and mineral mixture provided "better" antioxidant protection than the antioxidants administered individually if one considers all of the oxidative stress indices measured. However, one indicator, BP, did indicate that the antioxidant mixture might have been more effective than individual antioxidants in reducing oxidative stress.

In conclusion, people who work and recreate at moderate altitude may be at increased risk for oxidative stress damage and might benefit from an increase in dietary antioxidants; this agrees with the suggestion by Packer (1997) that bolstering antioxidant defenses may reduce exercise-induced oxidative stress damage. The results of our study also indicate that inferences regarding exercise and oxidative stress may depend upon the indicators examined and the composition of the antioxidant mixture ingested. A corresponding relationship between biochemical indicators of oxidative stress in breath, blood and urine could not always be ascertained, indicating the importance of including indicators of oxidative stress from more than one source when making such an assessment (Halliwell 1999 ). The lack of agreement among all indicators suggests the following two possibilities: either some indicators are not directly related to certain types of oxidative stress or the level of oxidative stress generated in this study was not sufficient to trigger increases in all indicators.

	ACKNOWLEDGMENTS

 
The authors acknowledge the advice and assistance of Greg Stoddard in the statistical analyses of the data.

	FOOTNOTES

 
¹ Supported by Ross Products Division, Abbott Laboratories, Columbus, OH, DataChem Laboratories, Salt Lake City, UT, the U.S. Naval Health Research Center, San Diego, CA and the University of Utah Graduate Fellowship Fund, Salt Lake City, UT.

² The views expressed in this article are those of the authors and do not reflect official policy or position of the Department of the Navy, Department of Defense, or the U.S. Government. Approved for public release, distribution unlimited. The assistance of U.S. Marine Corps personnel as subject volunteers for this study is acknowledged and appreciated.

⁴ Abbreviations used: -TE, -tocopherol equivalents; BP, breath pentane; LPO, lipid peroxides; 4-HNE, 4-hydroxynonenal; MDA, malondialdehyde; MRE, Meals, Ready to Eat; 8-OHdG, 8-hydroxydeoxyguanosine; ORAC, oxygen radical absorption capacity; RCW, Ration, Cold Weather; RE, retinol equivalents.

Manuscript received February 16, 1999. Revision accepted July 14, 1999.

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