Iron deficiency is often found among athletes, especially in those who perform a regular endurance training and in adolescents (5,12,18,20,22,23). Whereas there is no doubt about the benefits of iron supplementation in athletes with iron deficiency anemia, the results of studies on iron treatment because of low iron stores, as indicated by decreased ferritin levels but still normal hemoglobin concentration, are controversial (1,18,20). Several investigators did not find an improvement in exercise capacity although ferritin levels could be raised into the normal range after 2–8 wk of iron supplementation (11,19,21). In other studies, a significant improvement of V̇O2max and/or decrease in maximal blood lactate could be attributed to a significant increase in hemoglobin concentration, suggesting that the performance capacity of these athletes had previously been decreased because of an iron-deficient erythropoiesis (5,14,26). The assumption that only iron-deficient erythropoiesis or iron-deficient anemia (stage II or III of anemia;5), not iron depletion (stage I of anemia), causes a reduction of physical performance capacity in athletes is supported by the findings of Celsing et al. (4). They report reduced V̇O2max and endurance performance in athletes with iron deficiency induced by repeated venesections as long as they were anemic. When they had normal hemoglobin values again after retransfusion, they reached their normal V̇O2max and endurance capacity although ferritin levels were still decreased (4).
It is well known that endurance athletes have greater blood volumes than sedentary males and females because of an augmentation of red blood cell mass and plasma volume. Accordingly, in anemic female athletes, the red blood cell volume but not the plasma volume was significant lower than in nonanemic controls (2,29). The question arises whether iron-depleted athletes might have suboptimal red blood cell volumes because of a slight impairment of erythropoiesis not strong enough to cause obvious signs of iron-deficient erythropoiesis in peripheral blood. That could be the explanation for an improvement in endurance performance of iron-treated athletes without significant change of hemoglobin concentration opposed to the decrease in the placebo group in a study with female adolescent runners (24). Furthermore, the observation of iron-depleted bone marrows in runners with decreased serum ferritin points to that possibility (9,30).
However, the studies in athletes do not allow for conclusions on the effects of iron supplementation in stage I anemia on physical performance for several reasons: In some studies, athletes with ferritin levels > 20 μg·L-1 were included (11,28), and in most of the studies, the minimum therapeutic requirements (12-wk supplementation, 100-mg elemental iron daily (20)) were not met (11,13,14,26). Furthermore, red cell mass was never measured. It is conceivable that changes of plasma volume that may not parallel changes in erythropoiesis can simulate or mask effects of erythropoiesis on hemoglobin concentration. It was recently reported that increased red cell mass correlates with increased aerobic capacity after altitude training (15). Therefore, the purpose of this study was to test the hypothesis that high-dose iron supplementation over 12 wk leads to a significant augmentation of red blood cell volume in athletes with low serum ferritin and normal hemoglobin and that the physical performance capacity of these athletes would be increased after iron repletion.
A total of 51 young male and female athletes with serum ferritin levels (FER) < 20 μg·L-1 and Hb concentrations (HB) within the normal range (male: > 13.5 g·dL-1, female: > 11.7 g·dL-1) volunteered to participate in the study. They all were elite junior athletes and were sent to the lab for their annual health check as part of a support program for talented athletes. In a variety of individual endurance sports (middle- and long-distance running, triathlon, cycling, rowing, and swimming) and game sports, they all performed endurance training at least twice a week. After written-informed consent they were stratified according to sex and randomly assigned to an iron group or a placebo group. Ten subjects dropped out because of illness and injuries, one refused to take the medication after part of the study because of weight gain. Thus, 20 athletes remained in the iron group, 11 females (16.3 ± 1.8 yr, 170 ± 6 cm, 58.0 ± 6.1 kg), 9 males (17.6 ± 3.5 yr, 178 ± 6 cm, 66.3 ± 4.8 kg); and 20 were found in the placebo group, 12 females (15.9 ± 2.3 yr, 168 ± 7 cm, 57.8 ± 6.4 kg), 8 males (15.9 ± 1.6 yr, 182 ± 7 cm, 68.4 ± 13.2 kg). The resulting anthropometric data of each treatment group were for the iron group: 16.9 ± 2.7 yr, 174 ± 6 cm, and 61.6 ± 6.9 kg; and for the placebo group: 15.9 ± 2.0 yr, 174 ± 10 cm, and 62.0 ± 10.8 kg. None of the subjects showed any signs of illness that might have caused iron deficiency nor were they blood donors.
The iron group was treated with 567.7-mg ferrous-glycine-sulfate (gelatin-coated capsules) equivalent to 100-mg elemental iron twice a day for 12 wk. The placebo group received equal looking gelatin-coated capsules containing fructose. All subjects were instructed to take the capsules together with 200-mL orange juice on an empty stomach and to continue with their usual training program. The study was conducted double-blind with neither the investigators nor the subjects being aware of which subjects were receiving iron or placebo. To check toleration of the medicaments and adherence, subjects reported to the lab or were at least contacted by phone after 2 and 8 wk of treatment. At the same time, they returned a questionnaire concerning clinical symptoms and performance, such as headache; dizziness; loss of concentration; changes of skin, nails, or hair; digestive problems; loss of appetite; sleeplessness; muscle soreness or cramps; bad regeneration; and reduced maximal or endurance capacity. This questionnaire was also answered before and after treatment. Analysis of this questionnaire showed that the athletes experienced only few symptoms and that there was no significant change of symptoms throughout the study. A pill count was performed at the end of the study by one of the investigators. The protocol was approved by the ethic committee of the Medical Faculty of the University of Heidelberg.
Blood collection and analyses.
Before and after the 12-wk treatment, blood samples were drawn from an antecubital vein before the exercise testing at least 12 h after the athlete’s last exercise bout. From 5 mL drawn into an EDTA tube, HB, erythrocyte count (Erys), and mean corpuscular volume (MCV) were measured with a Coulter Counter (Coulter T 840, Coulter Electronics, Krefeld, Germany). Reticulocytes (Retics) were counted from air-dried brilliant cresyl blue stained blood smears. Eight mL of blood were centrifuged (3000 rpm, 15 min, 4°C), the serum immediately frozen for determination of serum iron (SI), FER, transferrin (TF), and saturation of transferrin (TFS). Photometrical analyses were used for SI (Ferrosin, Beckmann, Krefeld, Germany) and FER (enzyme immunoassay, Elias, Freiburg, Germany). TF was measured immune-nephelometrically (Nephelometer Analyzer II, Behring, Marburg, Germany).
Measurement of blood volume.
Blood volume was measured with carbon monoxide (CO) by a rebreathing method. The athlete ventilated a mixture of CO (mL CO = 0.85·kg body weight) in 5 L of O2 in a closed system. If necessary, O2 was refilled. The COHB fraction was measured in venous blood from antecubital veins with an automated system (270 CO-Oxymeter, CIBA-Corning, Fernwald, Germany) before and every 2 min while ventilating this mixture until a plateau was reached, usually near 5% COHB after 10–15 min. Total body hemoglobin (TBH) was calculated as:MATHaccording to Burge and Skinner (3), where K = barometric pressure/760 · [1 + (0.003669 · temperature)], MCO = volume of added CO in mL, DCOHB = difference between basal COHB and maximal COHB multiplied by 1.34 as 1.34 mL CO bind to 1-g HB.
Red blood cell volume (RBV), blood volume (BV), and plasma volume (PV) were calculated as:MATH MATH MATHMicrohematocrit was adjusted for trapped plasma and whole-body HCT by multiplication by the factors 0.96 and 0.91, respectively. To evaluate the CO rebreathing method the RBV of 10 subjects was measured on two consecutive days. Mean values were 2.47 ± 0.71 L (day 1) and 2.50 ± 0.67 L (day 2), respectively. There was no statistically significant difference. The test-retest correlation was 0.85.
Immediately before and after the treatment period, the subjects performed two treadmill tests on a motor-driven treadmill (Ergo ELG2, Woodway, Weil am Rhein, Germany). In both tests V̇O2, V̇CO2, and ventilation (V̇E) were measured continuously via breath-by-breath analysis with an automated computerized analysis system (OXYCONGAMMA, Mijnhardt, AE Bunnik, the Netherlands). Before the tests the paramagnetic O2 sensor and the infrared CO2 analyzer were calibrated with known gas concentrations. The turbine flowmeter for measuring V̇E was calibrated with a 3-L syringe.
In the first test, the athletes performed an incremental treadmill exercise for determination of V̇O2max, maximal capillary lactate concentration, maximal heart rate, and performance data at the individual anaerobic threshold (IAT) (27). Beginning with 8 km·h-1, the speed was increased by 2 km·h-1 every 3 min until volitional exhaustion. Before the test, during the last 20 s of each exercise step as well as 1, 3, 5, and 10 min after cessation of exercise 20 μL of capillary blood were drawn from the fingertip for lactate measurement with an automated system (ESAT 66.61, Eppendorf, Hamburg, Germany). Heart rate (HR) was recorded during the last 15 s of each exercise step from the continuously registered ECG (EK 53, Hellige, Freiburg, Germany).
The second test was conducted on a separate day to determine the maximal accumulated oxygen deficit (MAOD) as a measure of anaerobic capacity according to the procedure described by Medb / o and Tabata (17). At least 3 h after the submaximal part of the test, which was conducted for the determination of the individual linear relationship between speed and V̇O2, the athletes ran on the treadmill (8% inclination) with a speed corresponding to 120–140% of their V̇O2max until volitional exhaustion. Each athlete was tested with exactly the same treadmill speed before and after the 12-wk treatment. Anaerobic capacity was calculated as the maximal accumulated oxygen deficit (MAOD). According to Medb / o and Tabata (17), this is the difference between the measured oxygen consumption and the oxygen demand derived from linear extrapolation in the preceding submaximal test. Before, as well as 1, 3, 5, 10, and 15 min after cessation of exercise, 20 μL of capillary blood were drawn from the earlobe for lactate measurement. V̇O2peak for each test was calculated as 30 s average after reaching a plateau and the highest value was taken as V̇O2max.
All data are presented as mean value ± standard deviation (SD). Differences between means of variables before and after treatment were evaluated with the Wilcoxon signed-rank test. The Mann-Whitney rank-sum test was used to compare the treatment groups. Correlations were computed by the Pearson product moment. The level of significance was taken as P < 0.05.
There were no significant differences between the iron and placebo group concerning age, height, and weight.
Iron status and hematological data.
Iron status and hematological data before and after the 12-wk treatment are presented in Table 1. In the iron group, FER was significantly increased and TF significantly decreased after 12 wk, whereas these parameters did not change significantly in the placebo group. Posttreatment FER was significantly higher and TF significantly lower in the iron group compared with the values of the placebo group. SI and TFS did not change significantly throughout the study in neither group, but SI and TFS were always significantly higher in the iron group.
HB, HCT, Erys, MCV, and Retics had not changed significantly after treatment in either group. The iron group displayed a significantly higher HB than the placebo group in the posttreatment test.
Data of BV, RBV, PV, and TBH are shown in Figure 1. There was no significant change of BV, RBV, and TBH after treatment in either group nor was there any significant difference between the iron or placebo group. PV was significantly increased in the placebo group in the posttreatment test.
Performance data are presented in Table 2. After the 12-wk iron supplementation, there was a significant increase in the V̇O2max of the iron group, whereas there was no change in the placebo group. V̇O2max related to body weight only in the iron group showed a tendency to increase (P = 0.064). There were no significant differences between treatment groups. Maximal velocity in the incremental treadmill test showed a tendency (P = 0.058) to increase in the iron group and was significantly higher than in the placebo group after the 12-wk treatment. Maximal HR and maximal lactate remained unchanged in both groups.
In the anaerobic test MAOD and maximal lactate remained unchanged in both groups. Only in the iron group O2 consumption and time to exhaustion increased significantly. MAOD, O2 consumption, and time to exhaustion were significantly higher in the iron group compared with the placebo group in the pretreatment test. After treatment these differences were significant only for O2 consumption and time to exhaustion.
In both treatment groups, there was a significant correlation between V̇O2max and RBV (iron group: r = 0.506, P < 0.05, placebo group: r = 0.514, P < 0.05). There was no significant correlation between the individual changes in V̇O2max and RBV (Fig. 2) nor between the individual changes of V̇O2 in the MAOD test and RBV. Furthermore, there were no significant correlations between the individual changes in HB and the individual changes in ferritin or with the individual changes in V̇O2max, nor did the ferritin variations correlate with the V̇O2max variations.
When divided into male and female athletes, the results did not show important differences compared with those described above for the two genders combined. Remarkable, however, was that in the male placebo group velocity as well as V̇O2 at the IAT were increased after the 12-wk treatment (12.5 ± 1.7 vs 12.0 ± 1.7 km·h-1 and 48.9 ± 5.9 vs 46.2 ± 6.3 mL·kg-1·min; iron group: 13.6 ± 1.4 vs 13.4 ± 1.4 km·h-1 and 50.7 ± 4.1 vs 51.1 ± 2.7 mL·kg-1 ·min).
In the present study, the serum ferritin levels of nonanemic iron-depleted athletes were within the normal range after 12 wk of iron supplementation but the iron repletion did not lead to an increase in erythropoiesis and red blood cell volume remained unchanged. However, only in the iron-treated athletes, not in the placebo group, did V̇O2max and O2 consumption in the MAOD test increase significantly. Therefore, we conclude that the maximal aerobic capacity of young elite athletes with low serum ferritin and normal hemoglobin can be improved by iron supplementation without increasing the O2-carrying capacity.
In recent years, several investigations dealt with the frequent finding of iron deficiency in trained athletes. Whereas there is common agreement that iron-deficient anemia needs iron supplementation, the benefit of iron treatment exclusively because of low serum ferritin has not yet been proven. It seems that only athletes with iron-deficient erythropoiesis indicated by serum ferritin < 20 μg·L-1, transferrin saturation < 16%, and normal hemoglobin, a stage II anemia (5), experience a significant improvement of their exercise capacity after iron supplementation together with an increase in hemoglobin concentration (1,11,14,26). There were no significant changes in the exercise tests of athletes with isolated low serum ferritin, a stage I anemia (13,19,21,28). However, in these studies the serum ferritin levels below which the athletes were considered “iron deficient” vary considerably from < 20 μg·L-1(13,19) to < 35 μg·L-1(21), and the recommendation of a prolonged treatment period (≥3 months) with at least 100-mg ferrous iron daily was not met (20). This might be the reason for the rather small increases in serum ferritin (11,13,14,26). Only Newhouse et al. (19), Rowland et al. (24) and Telford et al. (28) reported ferritin increases of at least 15 μg·L-1 after iron supplementation. Whereas Rowland et al. (24) describe an improved endurance exercise performance in the iron-repleted female high school runners, Newhouse et al. (19) and Telford et al. (28) did not find significant changes of aerobic and anaerobic performance capacity after iron supplementation, but in the study of Telford et al., the initial serum ferritin was rather high with < 30 μg·L-1 (19.8 ± 8.4 μg·L-1).
The athletes of the present study were iron deficient with FER < 20 μg·L-1, TFS >16%, and normal HB. As SI and, consequently, TFS already at the beginning of the study were significantly lower in the placebo group than in the iron group, iron deficiency seemed a bit more marked in the placebo group, but both groups showed a stage I anemia. However, SI is the least reliable parameter of all measures of iron status as it shows circadian as well as day-to-day variations (5), so that the significant differences in SI and TFS between treatment groups probably are not important for the findings of the study. After a prolonged treatment of 12 wk with twice a day 100-mg ferrous iron, the iron group could be considered iron repleted with a significant mean increase by 20.1 μg·L-1 in FER opposed to the slight statistically not significant decrease in FER in the placebo group. HB did not change significantly in either treatment group, and the significantly lower HB in the placebo group compared with the iron group could most likely be attributed to the significant increase in the plasma volume of that group. It could be excluded that an increase in erythrocyte mass after iron supplementation was hidden by a simultaneous increase in plasma volume with help of the additional measurement of red blood cell volume besides the determination of HB.
Although iron repletion did not lead to an increase in oxygen carrying capacity, there was a significant increase in the maximal aerobic capacity of the iron-supplemented athletes indicated by a slight but significant increase in V̇O2max and a significant increase in the O2 consumption in the MAOD test after iron supplementation. Apparently, the increase in O2 consumption lead to a significant improvement of the performance (time to exhaustion) in this highly intensive test as the anaerobic capacity remained unchanged. Already at the beginning of the study, MAOD as well as time to exhaustion and O2 consumption were significantly lower in the placebo group compared with the iron group. After treatment, only the differences in O2 consumption and time to exhaustion but not in MAOD were statistically significant. However, it does not seem likely that a better pretreatment training condition of the iron group could be the explanation for the improvement in that group.
As performance at the individual anaerobic threshold had not changed significantly after iron treatment, an unchanged submaximal aerobic performance capacity can be assumed. It is not known why only the male placebo group improved performance at the individual aerobic threshold. However, the significant increase in velocity and %V̇O2max at the individual anaerobic threshold of that group is considered to be a training effect. As all subjects had different coaches and training programs some variability of training effects occurred.
The significant correlation between RBV and V̇O2max is in agreement with the results of other investigators (2,25). In the present study, the individual changes in V̇O2max did not correlate with the individual changes in RBV, a finding that gives further support to the assumption made above that the increase in the maximal aerobic capacity of the iron-treated athletes was not caused by an augmentation of erythrocyte mass. The possibility cannot be excluded that the CO-rebreathing method is not that sensitive to detect small increases of RBV after iron repletion which might be important for aerobic performance capacity. However, there exist further physiological explanations for an improvement of aerobic capacity after iron repletion.
Several studies with rats have shown that iron deficiency impairs aerobic capacity not only because of decreased oxygen delivery with diminished HB and red blood cell mass but also because of an iron depletion of the iron-containing compounds in solid tissue such as the cytochromes, myoglobin, catalase, peroxidase, the iron-sulfur proteins, metalloflavoproteins, or enzymes that require iron or haem as a cofactor, for example, aconitase, an enzyme of the tricarboxylic acid cycle (6,7,10). Davies et al. (7) made young weanling rats iron deficient by feeding them an iron-deficient diet. After transfusion of packed erythrocytes the rats’ HB was normalized but time to exhaustion in an endurance test was still markedly decreased. Also, they did not quite reach the V̇O2max measured before feeding the iron-deficient diet although it was dramatically increased compared with the iron-deficient anemic status. In another study, Davies et al. (8) found that HB increased substantially before any improvements in muscle oxidative capacity occurred when they followed the course of dietary repletion of severely iron-deficient rats. Taking the results of both studies together, it was concluded that these deficits could be attributed to a still impaired muscle oxidative capacity (7).
There are only few studies in which muscle enzyme capacities were measured in iron-deficient humans. Celsing et al. (4) did not find any significant changes in the activities of cytochrome c oxidase nor in glycolytic or oxidative enzymes. However, the activity of the only iron-depending enzyme measured, cytochrome c oxidase, was only 81% of the initial value in the vastus lateralis and 73% in the deltoideus, but this reduction was not significant. Newhouse et al. (19) did not find significant changes in muscle enzyme activity either but only measured non-iron-containing enzymes.
The results of the present study suggest that V̇O2max as well as O2 consumption in the MAOD test were improved after iron supplementation because of an increased muscle oxidative capacity. The findings of a reduced total O2 consumption during exercise in iron-deficient athletes and the reduction of maximal lactate concentrations after iron repletion in other investigations lead to similar assumptions (26). It does not seem likely that iron supplementation longer than 12 wk would lead to a significant increase in RBV as it could be shown in rats that HB is increased before improving muscle oxidative capacity (8,16).
Based upon the findings of the present study, it was concluded that iron supplementation in adolescent athletes with isolated low serum ferritin should be recommended not only to prevent anemia but also to treat an impaired aerobic performance capacity. Iron supplementation with twice a day 100-mg elemental iron (567.7 mg ferrous-glycine-sulfate) taken on an empty stomach for 12 wk seems to be sufficient to serve both reasons. Apparently, because erythropoiesis was not affected and red blood cell volume remained unchanged, the reason for the improvement of V̇O2max and O2 consumption in the MAOD test in the iron-treated athletes could be an increased muscle oxidative capacity. Detailed mechanisms, however, remain to be proven in humans.
Supported by the Bundesinstitut für Sportwissenschaft Cologne, Germany VF 0407/01/95.
Address for correspondence: Birgit Friedmann, Medical Clinic and Policlinic, Department of Internal Medicine, Division of Sports Medicine, University of Heidelberg, Im Neuenheimer Feld 710, 69120 Heidelberg, Germany; E-mail: firstname.lastname@example.org.
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