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Symposium: Nutrition and Exercise
Exercise and Iron Status1
CONNIE M. WEAVER2 AND SUJATHA RAJARAM
Department of Foods and nutrition, Purdue University, West Lafayette, IN 47907
ABSTRACT Total iron losses in feces, uriñeand sweat
in endurance-trained athletes are ~1.75 mg/d (com
pared with the reference value of 1 mg/d) in males and
~2.3 mg/d (compared with the reference value of 1.4
mg/d) in females because of the additional iron losses
with menses. Therefore, it is not surprising that many
investigators report that iron deficiency is a common
problem in athletes who do not increase their iron intake
above that of the general population. Recently, several
observations of iron deficiency associated with mild
exercise have been reported. Investigation of the extent
of iron loss and utilization in individuals exercising for
fitness is needed. Because compromised iron status
can affect athletic performance as well as general
health, including immune functions, cognitive devel
opment and ability to thermoregulate, it is advisable to
emphasize meeting the recommended dietary allow
ances for iron during exercise training. J. Nutr. 122:
782-787, 1992.
INDEXING KEY WORDS:
•exercise •iron status •athletic performance
•iron-deficiency anemia •humans
Iron-deficiency anemia is the leading nutritional
deficiency in the United States despite the widespread
use of iron enrichment and fortification programs. Iron
deficiency is usually attributed to inadequate iron in
takes,-high demands in some population groups, such
as during the adolescent growth spurt and women
during child bearing years; blood loss and inadequate
absorption. Increasingly, compromised iron status is
associated with exercise training. Whether this obser
vation is due solely to increased iron loss or partly to
an increased demand or represents a redistribution of
iron rather than a true deficiency is not entirely certain.
Whatever the phenomenon, signs of reduced iron sta
tus are occurring even after short periods of mild fit
ness-type exercise.
The reverse of the exercise-iron status relationship
might be that as iron status declines, athletic perfor
mance is reduced. There is convincing evidence from
both animal and human studies that iron deficiency
0022-3166/92 $3.00 ©1992 American Institute of Nutrition.
reduces physical work capacity. Both physical work
and exercise would require additional iron for oxygen
transport and cytochrome-mediated ATP production.
IRON DEFICIENCY
Iron deficiency progresses in three stages: 2) iron
stores in the bone marrow, liver and spleen are de
pleted; 2) erythropoiesis diminishes as the iron supply
to the erythroid marrow is reduced and 3) hemoglobin
production falls, resulting in anemia. The clinical
characteristics of these three stages are given in Table
1 as are methods for assessing associated iron status.
It is inadvisable to use a single status measurement
for detecting iron deficiency because of the enormous
intrasubject variability in these measurements. A
practical manual of procedures for measuring iron
status was prepared by the International Nutritional
Anemia Consultive Group (1).
The prevalence in the United States of the third
stage of iron deficiency, anemia, as assessed in the Sec
ond National Health and Nutrition Examination Sur
vey (NHANES II)3 from 1976 to 1980 (3), was 8.8%
of women 25-44 y of age when hemoglobin values of
< 120 g/L was used as the criterion for anemia. Inci-
1Presented as part of a symposium: Nutrition and Exercise,given
at the 75th Annual Meeting of the Federation of American Societies
for Experimental Biology, Atlanta, GA, April 22, 1991. This sym
posium was sponsored by the American Institute of Nutrition and
supported in part by grants from Proctor and Gamble Company,
the Coca Cola Company, the Quaker Oats Company, Ocean Spray
Cranberries, Inc., Bronson Pharmaceuticals, NPH, and Hoffman
LaRoche. Guest editors for this symposium were L. P. Packer, De
partment of Molecular and Cell Biology, University of California,
Berkeley, CA and V. N. Singh, Clinical Nutrition, Roche Vitamins
and Fine Chemicals, Nutley, NJ.
2To whom correspondence should be addressed: Department of
Foods and Nutrition, Purdue University, Stone Hall, West Lafayette,
IN 47907.
3Abbreviations: NHANES II, Second National Health and Nu
trition Examination Survey; TIBC, total iron-binding capacity; 2,3
BPG, 2,3 bisphosphoglycerate; TS, transferrin saturation; VOjm„,
maximal oxygen consumption; RDA, recommended dietary allow
ance.
782
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SYMPOSIUM: NUTRITION AND EXERCISE 783
TABLE 1
Assessing iron deficiency
Stage of deficiency Affected clinical indicator Measurement
I. Iron-deficient stores
II. Iron-deficiency erythropoiesis
III. Iron-deficiency anemia
Plasma ferritin <12 Mg/L
Transferrin saturation (TS) < 16%
Total iron-binding capacity (TIBC) > 4000 ^g/L;
Serum iron < 500 fig/L, Red cell distribution
width > 15%
RBC protoporphyrin > 700 /
Hemoglobin < 120 gL
Hematocrit < 0.36%
Immunoradiometric assay (IRMA); Diagnostic
Products, Los Angeles, CA; Cat. # IK Fe 1,
# IKFeS
Calculation (réf.1)
Sigma Chemical, St. Louis, MO Cat. # 565A
Coulter Counter
Fluorometric method (réf.2)
Cyanmethemoglobin assay; Sigma Chemical,
St. Louis, MO; Cat. # 525A
Heparinized capillary tubes
dence of stage I iron deficiency was 25.5% in women.
In response to concern over the connection between
dietary fat and cardiovascular disease, many individ
uals have reduced their consumption of beef and other
red meats. This trend may increase the incidence of
iron deficiency anemia in NHANES III.
Symptoms of iron deficiency include pallor, weak
ness, fatigue, dyspnea, palpitations, reduced capacity
to thermoregulate, paresthesia and a reduced capacity
for work. An adaptive mechanism of anemia is in
creased cardiac output, as viscosity thins with a low
red blood cell concentration. This may ameliorate
some of the symptoms of anemia. However, with ex
ercise, a further increase in cardiac output to meet the
increased oxygen demands is not possible. Hypoxia
ensues, which can reduce work capacity and prolong
recovery from exercise.
IRON STATUS IN ATHLETES
Reduced iron status in athletes (primarily runners)
has been documented by Newhouse and Clement (4).
They reviewed 21 studies with a total number of 3730
subjects. Only one study failed to demonstrate a high
incidence of low hemoglobin values. Consistently, a
high incidence of decreased serum ferritin values are
reported in endurance athletes ranging from 3 to 82%.
Even nonendurance athletes exhibit low serum ferritin
values. In one study (5) 15.6% of 45 female college
athletes who had normal ferritin levels preseason
ended the season with a serum ferritin concentration
of < 12 ng/L. Total serum iron and total iron-binding
capacity (TIBC)decreased significantly after only 2 wk
and ferritin levels decreased 50% after 4 wk of inten
sive 8 h/d physical training in men and women aged
18-20 y (6).Similarly, after 6 wk of anaerobic strength
training, serum ferritin decreased significantly by 35%,
although serum iron and transferrin saturation (TS)
were unaltered (7).
There is some evidence that ferritin progressively
decreases with each training season. For example,
Diehl et al. (8)reported decreases in ferritin in female
field hockey players of 8, 37 and 30% in seasons 1, 2
and 3, respectively, which reduced serum ferritin con
centrations from 25 to 17 /¿g/Lover the 3 y. By the
third year, hemoglobin and hematocrit values had also
decreased significantly. Although serum ferritin levels
increased somewhat between seasons, the athletes
failed to adapt to training.
Premenopausal women and adolescent athletes are
of particular concern because of the blood loss asso
ciated with menses in the former and the extra demand
with increasing blood volume and lean muscle mass
in the latter. Iron depletion has been reported in up
to 50% of adolescent female athletes and 17% of male
runners (9). As with adult athletes, prevalence of iron
deficiency increases during a season of endurance ex
ercise training. Mean serum ferritin in adolescent girls
fell from 26.6 to 14.0 ng/L during a competitive season
of cross-country running (10). By contrast, nonendur
ance swimming did not result in changes in serum fer
ritin during the training season (11).
EXERCISE AND IRON STATUS OF
NONATHLETES
Few studies exist on the effect of exercise training
or fitness-type exercise on previously sedentary indi
viduals. Thus, it is not surprising that results are in
conclusive. Comparisons are difficult because the
studies vary considerably with regard to the age of the
subjects, type of exercise and the duration of exercise.
Kilbom et al. (12) found small decreases in hemoglobin
and hematocrit values and a 25% decrease in serum
iron in adult women 19-64 y of age as a result of bi
cycle ergometer training at 70% maximal aerobic
power. However, Wirth et al. (13) showed no signifi
cant change in hemoglobin, hematocrit or serum iron
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784 WEAVER AND RAJARAM
in previously untrained college women who were on
a training regimen of three 20-25 min. bicycle work-
outs/wk for 10 wk when data were compared with
values from control subjects. Serum ferritin was not
measured in this study.
In another study, a decrease in serum ferritin but
an increase in hemoglobin concentration was reported
after 6 wk of aerobic fitness-type exercise by previ
ously untrained women (14). However, despite the
initial increase in hemoglobin, levels returned to near
normal by week 13 of the exercise program. Serum
ferritin levels remained lower than initial values
throughout the study and hematocrit decreased only
between weeks 6 and 13. Changes in serum ferritin
suggested that a compromise in iron stores occurred
that seemed to stabilize after 6 wk of exercise. Because
stores did not further deplete and because none of the
subjects developed stage II or III iron deficiency, the
authors concluded that a physiological adaptation had
occurred.
Similarly, serum ferritin and hemoglobin initially
dropped, then stabilized, after 4 of 12 wk of moderate
aerobic exercise intervention in college age women
(15). However, the initial drop in these values indi
cated that stage III iron deficiency had been reached
in 9 of 14 women. Thus, if a plateau in iron status
measurements occurs at a level of iron-deficiency ane
mia, a compensatory reaction rather than an adapta
tion is implied.
EVIDENCE OF IRON DEPLETION WITH
EXERCISE IN RATS
Use of an animal model allows study of iron in tis
sues not accessible in human studies, as well as careful
control over diet and exercise protocol. The effect of
exercise on the uptake, redistribution and excretion
of iron was studied by Strause et al. (16) in iron-suf
ficient rats. Strenuous exercise did not reduce hemo
globin concentrations but did increase iron absorption
and stimulated the redistribution of storage iron from
the liver and spleen to the heart and for myoglobin
synthesis in muscles. Similarly, lower iron stores in
the liver, spleen and gastrocnemius of exercising com
pared with sedentary rats were observed (17). Hemo
globin concentration and hematocrit levels were in
creased in male, but not female, rats compared with
sedentary controls (18). Contrary to the findings of
Strause et al. (16), total fecal iron increased and ap
parent iron absorption decreased. Exercise had no ef
fect on iron status or iron absorption in female rats
fed adequate diets. Thus, exercise has been reported
to decrease, to increase and to have no effect on iron
status in rats. These inconsistencies could be due to
differences in severity and duration of exercise, gender
studied and/or the length of the training regimen.
CAUSES OF EXERCISE-INDUCED
IRON DEFICIENCY
The production of a true iron deficiency by exercise
has been questioned. Some refer to the decrease in he
moglobin observed during exercise training, especially
an initial, transient anemia, as sports anemia. This
term refers to the apparent hemoglobin concentration
decrease by hemodilution when erythropoiesis cannot
keep pace with the expanding blood volume induced
by the oxygen demands of exercise. Although increases
in blood volume with endurance training has been
documented (19), changes in blood volume as reflected
in serum albumen concentrations have not always been
observed (15)or were too small to account for changes
in hemoglobin (6, 8). For example, if total iron stores
had remained constant in the female field hockey
players studied by Diehl et al. (8), blood volume ex
pansion would have had to have been 58% to account
for the observed 37% drop in serum ferritin over a
season. Schobersberger et al. (7) also ruled out hemo
dilution as an explanation for lowered hemoglobin
concentrations during 6 wk of strength training be
cause the drop in hemoglobin was not a rapid, initial
response and packed cell volumes and red cell counts
increased toward the end of the intervention. More
over, decreases in TS and increases in TIBC with
training (20) cannot be explained by hemodilution.
Another explanation for a decrease in hematological
values with exercise that could work in concert with
hemodilution to create an initial anemia is increased
intravascular hemolysis of mainly old red blood cells
due to the impact of exercise (foot strike hemolysis)
(21) or to contraction of large muscle masses such as
in swimming (22). Increased hemolysis stimulates
erythropoiesis. Higher concentrations of young red
blood cells in circulation, which have higher concen
trations of 2,3-bisphosphoglycerate (2,3-BPG), which
in turn lowers the affinity of hemoglobin for oxygen,
and decreased serum haptoglobin have been observed
in endurance-trained athletes (7). The impaired bind
ing of oxygen to hemoglobin can result in the same
tissue oxygen delivery as at higher hemoglobin levels
in nonexercising individuals in the short term. The
increased 2,3-BPG can suppress erythropoiesis. Hall-
berg and Magnusson (23) suggested that iron is not
lost due to hemolysis. Rather, haptoglobin-hemoglo-
bin complex formation prevents excretion of free he
moglobin in the urine. The complex is taken up by the
hepatocytes and the iron is conserved. This shift in
red cell catabolism from the reticuloendothelial system
to the hepatocytes may explain the observed reduced
serum ferritin concentrations in athletes. Magnusson
et al. (24) concluded from their study in runners that
a true iron deficiency did not exist because sideroblast
counts, red cell indices and red cell protoporphyrin
were normal, suggesting that erythropoiesis was not
limited. In opposition to this theory, others (7) have
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SYMPOSIUM: NUTRITION AND EXERCISE 785
observed no change in hemoglobin affinity for oxygen,
red cell 2,3-BPG levels or mean red cell age as deter
mined by glutamate-oxalacetate transaminase activity
despite decreases in serum haptoglobin and ferritin
and hemoglobin during strength training.
A true iron deficiency associated with exercise
would exist if exercise increased losses from the body,
lowered the amount of iron that could be utilized
from the diet or increased demand from myoglobin
and iron-containing respiratory enzymes (Fig. 1). Al
though reduced serum haptoglobin concentration in
athletes does imply intravascular hemolysis, iron is
not necessarily lost from the body. However, iron
losses in the feces, which would indicate gastrointes
tinal bleeding, and hemoglobinuria from intravascular
hemolysis have been reported. Stewart et al. (25) used
the HemoQuant assay to assess fecal heme compounds
and found levels increased in 20 of 24 runners after a
race; 7 of these runners lost >3 mL of blood (2 mg of
Fe) per day, which would double usual iron losses.
Similarly, 9 of 20 female high school runners had in
creased fecal iron and 7 of these 9 had stage II iron
deficiency (26). No urinary iron losses were observed
in this study. Hematuria was observed after a mara
thon race in 9 of 50 subjects, however (27). Hematuria
may be the result of bladder wall trauma during ex
ercise; iron may also be lost in the urine due to in
creased transferrin excretion after exercise or brisk in
travascular hemolysis (28). Urinary iron losses aver
aging 0.18 mg/d have been reported (24). Sweat iron
losses could exceed 0.6 mg/d for athletes excreting 3
L of sweat at 0.21 mg/L (29).
Weak evidence exists that iron absorption by ath
letes may be lower than for nonathletes. Ehn et al. (30)
reported that endurance runners absorbed only 16%
of an oral 59Fedose compared with 30% of iron-defi
cient control subjects, but the difference was not sta
tistically significant with a sample size of only eight
per group. The biological half-life of the 59Fein athletes
was much shorter than for the control subjects; 2 mg
of Fe was eliminated per day in these athletes.
IRON STATUS AND ATHLETIC
PERFORMANCE
Anemia can impair exercise performance because
reduced hemoglobin concentration is associated with
a reduced blood oxygen content. As hemoglobin con
centration decreases, a nearly linear reduction in max
imal oxygen consumption (VO2max)and exercise ca
pacity ensues (31). Blood transfusions to correct ane
mia result in an almost immediate improvement in
work performance (32). Additionally, postexercise
láclatelevels increase and persist longer as hemoglobin
decreases (33), indicating reduced aerobic capacity.
Partially offsetting this for the short term is a decrease
IRON LOSSES
IN SWEAT INCREASED
DEMANDFOR
MYOGLOBIN
AND IRON
CONTAINING
RESPIRATORY
ENZYMES
EXERCISE
INTRAVASCULARHEMOLYSIS
HAPTOGLOBIN CONCENTRATION)
IRON LOSSES IN FECES, URINE
DEPLETED IRON STORES
(LOW SERUM FERRITIN)
ANEMIA
(LOW HEMOGLOBIN)
FIGURE 1 Possible mechanism for exercise-induced iron
deficiency.
in hemoglobin-oxygen affinity due to an increase in
2,3-BPG. However, endurance performance requires
oxygen utilization for phosphorylation for prolonged
periods. Pate (34) suggested that hemoglobin concen
trations for optimal oxygen delivery should exceed
150-160 g/L.
Low serum ferritin values are not associated with
an impairment in exercise performance or work ca
pacity in adults (32). An exception to this generaliza
tion has been reported in adolescents (11).
IRON STATUS AND ITS EFFECT ON
EXERCISE IN RATS
In rats, anemia also affects performance. Edgerton
et al. (35) reported that on 12 of 13 occasions in four
separate experiments, the capacity of iron-depleted
rats to endure an exhaustive endurance test was di
rectly related to their hemoglobin concentration and
percentage packed cell volume. Treadmill performance
was more negatively affected by iron deficiency in male
than in female rats (36). Iron-deficient exercised rats
had a higher fractional iron turnover rate and VO2m«
than sedentary controls (37). Similarly, VO2 maxand
exercise endurance capacity was reduced in anemic
rats (38). Training improved endurance and muscle
oxidative enzymes.
INFLUENCE OF DIETARY IRON INTAKE ON
IRON STATUS AND ATHLETIC
PERFORMANCE
To the extent that exercise increases iron losses,
athletes become more vulnerable to a negative iron
balance. The only practical approach to increasing iron
balance is to increase absorbable iron in the diet, which
may also improve athletic performance through in-
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786 WEAVER AND RAJARAM
creasing hemoglobin levels. Although dietary surveys
of male athletes as reviewed by Pate (34)have generally
concluded that athletes receive the recommended di
etary allowance (RDA) for iron, not all athletes do,
especially menstruating females. For example, the av
erage iron intake in female distance runners was 12.5
mg/d (39), which is well below the RDA of 15 mg/d.
Of the 21 female and 50 male recreational triathletes
studied by Worme et al. (40), 43% of the women and
2% of the men ingested less than the RDA for iron.
Iron intake averaged only 43% of the RDA in female
high-school runners (11). An increased demand in iron
due to exercise would increase the proportion of in
dividuals with a relative iron deficiency.
For individuals who have iron status indices indi
cating iron deficiency, improvement in these values
with iron supplementation would provide strong ev
idence for a true iron deficiency. In some studies, iron
supplementation has resulted in an improvement in
both hematological measurements and performance.
In Maharastrian women, 60% of whom were mildly
to moderately iron deficient, hemoglobin status im
proved by 50 g/L, serum ferritin by 35.6 Mg/L,TS by
16% and serum iron by 454 Mg/Lafter 10 wk of iron
supplementation at 115 mg/d (41). During this inter
vention period, performance on the Harvard step test
improved significantly. In a study of adolescent run
ners by Rowland et al. (42), 14 subjects with stage I
iron deficiency responded to supplementation with
improved ferritin values and improved treadmill en
durance values whereas control subjects decreased in
both. No change in VO2maxwas observed between the
groups. In contrast to this study, both serum ferritin
and VO2 maximproved in mildly exercising college
women given 50 mg Fe/d compared with control sub
jects (43).
In some studies, the increase in work capacity is
not matched by increases in hemoglobin (44). Thus, a
significant, but less dramatic, nonhemoglobin effect
on physical work capacity must be operational. Evi
dence in nonanemic iron-depleted rats (45) suggests
that decreased iron-dependent biochemical factors es
sential for aerobic metabolism may be the cause of
impaired work performance. However, in humans
made iron deficient but not anemic, no significant
changes in iron-dependent enzymes of skeletal muscle
were observed (46). Nevertheless, from evidence in
rats (37), training might improve tissue oxidative ca
pacity. A very rapid, although minor, response (<16
h) to iron injections in exercise endurance in iron-de
ficient rats is suggestive of a role for ionic iron as a
cofactor for an enzyme because hemoglobin and elec
tron transport iron enzymes would require more time
for synthesis (47).One such enzyme could be aconitase
hydratase of the trichloroacetic acid cycle.
Iron supplementation has been reported to improve
iron status without improving exercise performance
in other studies (48). However, 2 wk of 300 mg Fe/d
iron therapy did significantly reduce blood lactate lev
els after maximum exercise compared with control
subjects.
Failure to show an improvement in iron status of
iron-deficient athletes may be explained by iron ther
apy that is insufficient in absorbable iron. Nickerson
et al. (26) found that 180 mg Fe/d, but not 50 mg Fe/
d, was adequate to prevent iron deficiency in female
adolescent runners. Supplementation of a residence
hall menu with meat snacks to bring the dietary iron
intake near the RDA was more effective than 50 mg
Fe/d as ferrous sulfate in ameliorating the sports ane
mia observed in mildly exercising women (15). This
observation and the lower ferritin values of vege
tarian (7.4 ±1.4 itg/L) compared with meat-eating
(19.8 ±4.2 Mg/L)runners (49) confirms the value of
meat with its heme iron content and nonheme-iron-
absorption-enhancing factor in supplying absorbable
iron.
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