International Journal of Sport Nutrition, 1992, 2, 376-385

Effects of Low Ferritin Concentration on Endurance Performance

John J. Lamanca and Emily M. Haymes

To determine the effects of depleted iron stores on endurance performance and blood lactate concentration, eight active women with normal (>26 ng/ ml) and eight with low (<I2 nglml) plasma ferritin concentrations were studied while performing a V02max and an endurance test (80% V0,max) on a cycle ergometer. The low femtin group had significantly lower serum iron concentration and transferrin saturation and higher TIBC than the normal femtin group. Mean V02max was not significantly different between groups. No significant difference was found in total time to exhaustion during the endurance test for low (23.2 min) and normal (27.0 min) femtin groups; however, the normal femtin group exercised 14% longer. Blood lactate concentrations following the VOzmax and endurance test did not differ signifi- cantly between groups. Food diaries revealed lower daily absorbable iron intake by the low femtin group compared to the normal ferritin group. Ferritin concentration was significantly related to absorbable iron (c .72) and total iron (p.70) intake. The results suggest that women with depleted iron stores who are not anemic may have less endurance, but do not have higher blood lactate during exercise than women with normal iron stores.

Iron depletion, usually defined as a low serum ferritin level, is a common problem in women athletes and is especially prevalent among those involved in distance running (1,7, 18,27,31). Although the incidence of depleted iron stores is very low in the general population of men (9), studies have reported low serum ferritin and little iron stored in the bone marrow of men distance runners as well (1, 12, 13). Low iron stores can ultimately lead to a reduction in hemoglobin concentration and iron deficiency anemia. Because hemoglobin is the main carrier of oxygen to the cells, low hemoglobin concentration would impair aerobic metabolism. The detrimental effects of iron deficiency anemia on physical perfor- mance are well documented (15, 28).

While the prevalence of depleted iron stores in endurance athletes is rela- tively high, the incidence of iron deficiency anemia is reported to be quite low (1, 7, 18) with a few exceptions (31). Most studies have found that maximal

John Lamanca is with the V.A. Medical Center, Philadelphia, PA. Emily Haymes is with the Department of Nutrition, Food, and Movement Sciences, 203 Montgomery Gym, Florida State University, Tallahassee, FL 32306.

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aerobic power of iron depleted subjects without anemia is not significantly re- duced (6, 26, 34). Myoglobin, the cytochromes, and several tissue enzymes involved in energy production contain iron. Prolonged iron depletion could lead to a reduction in tissue iron levels before anemia develops. Recent animal studies have suggested that depletion of tissue iron has a detrimental effect on endurance performance that is independent of the hemoglobin concentration (10, 11, 24).

Studies with human subjects have produced mixed results. Iron supplemen- tation of iron depleted female athletes with borderline hemoglobin resulted in reduced lactate following maximal exercise (34) and improved running endurance (33). On the other hand, Celsing et al. (6) found no reduction in the endurance of iron depleted men following blood retransfusion. Iron depletion in the study by Celsing and colleagues was produced by repeated phlebotomies and the men were iron depleted for only a few weeks. Many women athletes are in negative iron balance due to a low dietary iron intake that may have existed for several years. Celsing et al. (6) found that short-term reduction in iron stores had no effect on the activity of iron-containing proteins in muscle tissue. It is possible that a prolonged iron deficiency could reduce the synthesis of these same enzymes.

Because of the conflicting results of previous studies, more research on the effects of iron depletion on submaximal endurance performance is needed. The primary purpose of the present study was to examine the effects of iron depletion without anemia on submaximal endurance performance and blood lactate concen- trations of active women. The second purpose of this study was to determine whether low dietary iron intake was a possible cause of iron depletion in these women athletes.

Methods

The subjects for this study were selected from a group of 40 women recreational athletes from several Tallahassee area athletic and fitness clubs (e.g., track, triathlon, cycling, rugby). All of the women, ages 21 to 35 years, had k e n participating in aerobic training a minimum of 30 minuteslday, three or more times a week for at least 8 weeks prior to the study. After screening for iron status, 16 subjects were selected by one of the investigators who did not participate in the exercise testing. Eight subjects had normal ferritin concentrations (>26 ng/ ml) and eight had low plasma femtin concentrations (<I2 ng/ml) indicative of depleted iron stores. Prior to the study, all subjects were given a complete explanation of procedures and possible risks involved in the study, and all signed an informed consent statement. This study was approved by the Committee on the Use of Human Subjects at Florida State University.

Blood samples were collected between 8 and 10:30 a.m. following a 12- hour fast. Two 10-ml samples were obtained from an antecubital vein. One sample in a vacutainer containing no anticoagulants was allowed to clot. After the blood was centrifuged, serum was removed and placed in iron-free tubes for the analysis of serum iron and total iron binding capacity (TIBC). The other sample was obtained in a heparinized vacutainer. From this tube duplicate samples were removed for determining hemoglobin and triplicate samples were removed for measuring the hematocrit. The remaining blood was centrifuged and the plasma was frozen for later analysis of ferritin. Hemoglobin concentration and hematocrit were measured using the cyanmet hemoglobin method (Sigma Diagnostics) and

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microhematocrit technique, respectively. Hematocrit readings were corrected (0.96) for plasma trapped with the packed cells. Serum iron and TIBC were determined using a colorimetric method (30). Percent transfenin saturation was determined by computing the ratio of serum iron to TIBC. Femtin concentration was determined with a radioimmuno assay using a modification of the method of Luxton (22).

Physical characteristics of the subjects selected for the exercise tests were determined prior to testing. Body density was measured using the hydrostatic technique described by Katch et al. (19). Residual volume was measured using the helium dilution technique. Body fat was calculated according to the equation of Brozek et al. (5).

All subjects completed 3-day food diaries. They were instructed in the proper methods for measuring and recording food amounts. Nutrient intake was analyzed using the Nutritionist I11 computer software. Food iron bioavailability was calculated according to the method of Monsen and Balintfy (25).

Each subject completed two exercise tests, a maximal oxygen uptake test (V0,max) and a submaximal (80% V02max) endurance test, on separate days. On the days of the exercise tests the subjects reported to the laboratory at least 3 hours postprandial. They were asked to refrain from exercise for 24 hours preceding each test. Maximal oxygen uptake was determined on a Monark cycle ergometer using a continuous protocol described by McArdle et al. (23). Subjects pedaled the ergometer at 60 rpm and the intensity was increased 180 kpm every 3 minutes until the subject was unable to continue. Respiratory data and heart rates were sampled continuously throughout the test. Criteria used to establish VOzmax were two of the following: plateau of V02, heart rate equal to age- predicted maximum, and a respiratory exchange ratio (RER) greater than 1.1. Venous blood samples for measuring blood lactate were obtained from an antecu- bital vein before and 5 minutes postexercise.

Endurance was measured as the time to exhaustion on the cycle ergometer at afi exercise intensity that elicited 80% V02max. Subjects pedaled at a rate of 60 rpm until exhaustion, defined as the time at which they could no longer maintain a pedal frequency of 50 rpm. No verbal encouragement or indication of time was given during the test. Heart rate was monitored continuously throughout the test, and respiratory data were sampled continuously during the first 10 minutes of exercise and thereafter at 10-min intervals. Perceived exertion using the Borg scale (4) was measured at 10-min intervals. Venous blood samples were taken before and 5 minutes postexercise.

Respiratory samples were analyzed using a Vacumed dry gas meter and Applied Electrochemistry S-3A O2 and Ametek CD-3A C02 analyzers. The Rayfield computer-based system was used with an Apple IIe computer to calculate respiratory and metabolic data every 30 seconds. Heart rate was monitored using a Burdick Electrocardiograph. Lactate was determined by an enzymatic method (Sigma Diagnostics). Blood and dietary intake data for the two groups were analyzed using a two-way t test for independent means. Two-way ANOVA with repeated measures on the time factor was used to analyze physiological responses during the endurance test. Correlation coefficients were calculated between se- lected exercise, hematologic, and dietary variables. The .05 level of probability was accepted as significant.

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Table 1

Physical Characteristics of the Low and Normal Ferritin Groups

Low ferritin Normal ferritin

M SD M SD

Age (yrs) Height (cm) Weight (kg) Body fat (%) V0,max (Ilrnin)

(rnllkglmin) Maximal heart rate (bprn) Maximal RER

Note. n = 8 for each group.

Results

Physical characteristics of the two groups are presented in Table 1. There were no significant differences in age, height, weight, and percent body fat between the two groups. Both groups were similar in their exercise habits. Women in the low femtin group exercised 5.7 days/week for an average of 56 minuteslday while women in the normal ferritin group trained 5.9 days/week for an average of 57 minuteslday. All of the women ran an average of 16 mileslweek at an average speed of 7 mph. In addition, six women cycled, four swam, six participated in aerobics, three lifted weights, and one played rugby.

Iron status and intake of the subjects are presented in Table 2. Subjects for the two groups were selected so that plasma femtin concentrations would be significantly different. When compared to the normal ferritin group, the low fekitin group had significantly lower serum iron concentration and percent trans- femn saturation, and significantly higher TIBC. All of the women in the low femtin group had ferritin concentrations less than 12 nglml but no subject had a percenttransferrin saturation below 16%. Only one subject had a hemoglobin concentration below 13 gIdL, and her hemoglobin was 11.5 g/dL. Although the low fenitin group had a lower total iron intake than the normal ferritin group, the difference was not statistically significant (p=.08). Five women in the normal ferritin group and one in the low fenitin group were taking multiple vitamin with iron supplements. The absorbable iron intake of the normal ferritin group was higher than that of the low femtin group (p=.05). There were no significant differences in food iron, heme iron, and nonheme iron intakes between the groups. Ferritin concentration was significantly correlated with the absorbable iron (r=.72) and total iron intake (p.70). Percent transfenin saturation was also significantly correlated with the absorbable iron (p.56) and total iron ( p . 5 1) intakes. There were no other significant correlations between hematologic and dietary iron status.

There was no significant difference in VOzmax between the low femtin (41.7 f5.3 ml/kg/min) and normal fenitin groups (41.6 k7.9 ml/kg/min). Although

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Table 2

Iron Status and Average Daily Nutrient Intake of Low and Normal Ferritin Groups

Low ferritin Normal ferritin

M SD M SD

Hematocrit (%) Hemoglobin (gldL) Serum iron (ug1dL) TlBC (ugldL) Transferrin saturation (%) Ferritin (nglml) Total iron intake (rnglday) Food iron (mglday) Nonheme iron (mglday) Heme iron (mglday) Supplemental iron (rnglday) Absorbable iron (mglday) Protein (glday) Vitamin C (mglday)

Note. n = 8 for each group. *Significant at the .05 level of probability.

the normal ferritin group tended to have a higher blood lactate following the V02max test (8.4 a . 1 mM/L) than the low ferritin group (7.2 k1.3 mM/L), the difference was not statistically significant (P>.05). There were no significant correlations between V02max or blood lactate and ferritin or hemoglobin concen- tration.

Table 3 presents the results of the submaximal endurance test. Both groups exercised at slightly more than 80% V02max. There were no significant differ- ences in %VOpmax, intensity, heart rate, rating of perceived exertion, time to exhaustion, or postexercise lactate between groups. No significant correlations were found between blood lactate or time to exhaustion and ferritin or hemoglobin concentration. Exercise time was significantly related to the perceived exertion ratio (7=-.7 1).

Discussion

The primary purpose of this study was to determine whether iron depleted nonane- mic active women has less endurance than active women with normal iron status. Time to exhaustion on the endurance test was 14% less for the iron depleted group, but the difference between groups was not statistically significant. The large standard deviations in endurance performance of both groups makes it difficult to detect small differences between the groups. In terms of athletic performance, however, a difference in endurance of 3.8 minutes is of considerable

Low Ferritin Concentration / 381

Table 3

Results of Submaximai Endurance Test for the Low and Normal Ferritin Groups

Low ferritin Normal ferritin

M SD M SD

VO, (rnllkglmin) 34.4 2.7 34.8 5.7 % V0,max (%) 82.9 7.2 84.2 6.9 Heart rate (beatslrnin) 169 7 167 6 Exhaustion time (min) 23.2 9.8 27.0 11.7 Perceived exertion 16 2 17 8 Postexercise lactate (mMIL) 5.0 1.2 4.8 2.4

Note. n = 8 for each group.

practical importance. Celsing et al. (6) also did not find a significant difference in endurance performance between normal and nonanemic iron depleted states.

These results are in sharp contrast with those of Rowland et al. (33), who found reductions in endurance in nonanemic iron depleted subjects. One difference between the Rowland study reporting a detrimental effect of iron depletion and those that did not find significant differences is the age and maturity of the subjects. The studies that did not find significant differences in endurance used adult subjects. Rowland and colleagues (33) used young adolescent female runners. Extra iron (.38 mglday) is required during adolescent growth (17) for blood volume expansion and iron-containing tissue compounds (e.g., myoglobin, cytochromes) in growing muscles. Onset of the menses in adolescent girls in- creases iron loss, putting a greater strain on iron stores. We do not know how long our subjects had been iron depleted or whether any of them had been in an iron depleted state during growth.

The rat studies that reported significant reductions in endurance in iron deficient animals without anemia used young, growing rats fed iron deficient diets from the time they were weaned (10, 14). Reductions in endurance in the animal studies were linked to reduced myoglobin and cytochrome levels and mitochondria1 enzyme activity (11, 24). Failure to establish normal iron stores during growth may impair the formation of iron-containing compounds in the muscles and other tissues. Once growth is completed, depletion of iron stores may have little effect on iron-containing compounds in muscles. No significant reductions in myoglobin content and cytochrome oxidase activity were seen when adult animals were placed on an iron deficient diet for 300 days (20). Studies with adult human subjects are in agreement with the adult rat study. No reduction in muscle enzyme activity was observed in the men subjects of Celsing et al. (6), who were iron depleted for 4 weeks. Newhouse et al. (26) found no significant increase in muscle enzyme activity of iron deficient women after 8 weeks of iron supplementation.

The pedal frequency of 60 rpm used in the endurance test may not have been optimal for prolonged exercise. Although mechanical efficiency is optimal

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at pedal rates of 60 to 80 rpm, blood lactate and perceived exertion are higher at 60 rpm (8). Our subjects may have stopped exercising because of fatigue of the leg muscles. We found a significant negative correlation between exercise time and perceived exertion. Most of the women had blood lactates greater than 4mM at the end of the endurance test.

There were no significant differences in lactate concentration between the two groups following either the maximal or endurance tests. The results of this study support the previous findings of Celsing et al. (6) but are not in agreement with the results of Schoene et al. (34), who found a higher maximal lactate in iron deficient women prior to iron therapy. However, mean hemoglobin concentra- tion of the women in the Schoene study was lower (12.2 g/dL) than for the iron depleted women in the present study (13.8 g/dL).

The women in the low ferritin group had significantly lower serum iron and transferrin saturations and higher TIBCs than those in the normal ferritin group. TIBCs greater than 390 ug/dL are characteristic of iron deficient erythro- poiesis, but none of the women had transferrin saturations less than 16%. Four women had TIBCs above 400 ug/dL but only one had a transferrin saturation below 20%. Timing of blood sampling may have contributed to higher serum iron concentrations. Diurnal variations in serum iron are well documented, with the highest concentrations occurring in the morning (3). Blood samples in this study were obtained in the morning. It is possible that training may have masked low percent transferrin saturation in the low ferritin group. Elevated transferrin saturations have been found in women athletes during strenuous training, these saturations declining when training is reduced (2). Increases in serum iron concen- tration have been observed at the end of and during recovery from 45 minutes of strenuous exercise (16). The increase in serum iron concentration could be due to iron released from the reticuloendothelial system (29).

The iron depleted women in this study had lower total iron and absorbable iron intake than the women with normal iron status, which suggests that low iron intake may have been a factor in reducing iron stores in these athletes. This is further supported by the significant correlations between plasma ferritin and total iron and absorbable iron intake. Absorption of iron is three times greater from food sources containing heme iron than nonheme iron. Meat, fish, and poultry are heme iron sources and also enhance the absorption of nonheme iron.

Recent studies suggest that vegetarian runners are more likely to be iron depleted than runners who consume meat (35,36). Only one subject (low ferritin) in this study consumed a vegetarian diet, however, and she supplemented her food intake with an iron supplement. Because there were no significant differences in food iron or heme iron intake between the two groups, the most likely explana- tion for the greater iron intake of the normal femtin group was their greater use of iron supplements. Balaban et al. (1) recently reported that women runners who took iron supplements had significantly higher serum ferritin levels than women runners who did not take iron. Their results as well as those of the present study suggest that iron supplements may help prevent iron depletion in women runners.

Since the average iron loss for menstruating women is 1.5 mg/day, an absorbable iron intake of 1.1 mg/day would result in a negative iron balance of 0.4 mg/day. Assuming that normal iron storage for women is 400 mg, a loss of 0.4 mg/day would totally deplete the iron stores in 1,000 days, or approximately 3 years. Iron loss may be increased in runners due to gastrointestinal bleeding

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(32) and sweating (21, 35). Additional iron lost in the sweat and feces would accelerate depletion of the iron stores. One nglml of ferritin is the equivalent of 10 mg of stored iron (9). Because serum femtin was less than 10 ng/ml in the iron depleted group, it is likely that the women in this group had been in negative iron balance for more than 1 year. It is not known how long any of these women had depleted iron stores; however, the elevated TIBC in four women suggests they had reached the iron deficient erythropoiesis stage.

In summary, although there was a 14% difference in submaximal endurance performance between women athletes with low and normal ferritin concentrations, the difference was not statistically significant. There were also no significant differences in postexercise lactate concentration following either the maximal or endurance tests. Low absorbable iron intake by women athletes was associated with low ferritin concentration and depleted iron stores.

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