You are on page 1of 6

International Journal of Sport Nutrition and Exercise Metabolism, 2011, 21, 501-506

2011 Human Kinetics, Inc.

Impact of Iron Depletion Without Anemia on Performance


in Trained Endurance Athletes at the Beginning of a Training
Season: A Study of Female Collegiate Rowers
Diane M. DellaValle and Jere D. Haas
The objective of this study was to determine the impact of iron depletion without anemia on performance in a sample of
female collegiate rowers at the beginning of a training season (August 2008, January 2009, and September 2009). One
hundred sixty-five female collegiate rowers from 5 colleges and universities in central New York State participated in a
screening of iron status. Blood hemoglobin (Hgb), serum ferritin (sFer), and soluble transferrin receptor were measured to
determine prevalence of iron depletion and anemia. Rowers habitual moderate and vigorous physical activity, as well as
their best time to complete a 2-km simulated race during the previous 3 months, were self-reported. Sixteen rowers (10%)
were identified as anemic (Hgb <12.0 g/dl). Using a sFer cutoff of <20.0 g/L, 30% (n = 44) of the nonanemic rowers were
identified as iron depleted without anemia and reported 2-km times ~21 s slower (p < .004) than rowers with normal iron
status. Given the high prevalence of iron depletion reported in this and other studies, screening for low iron stores at the
start of a training program in female athletes involved in an endurance sport may be clinically useful. In this study, irondepleted rowers (sFer <2025 g/L) reported a decrease in performance time compared with those with normal iron stores.
Keywords: iron deficiency, physical performance, serum ferritin, female athletes, rowing training

Iron deficiency is the most prevalent nutrient deficiency in the world. In the United States, iron deficiency
with anemia affects 35%, and iron deficiency without
anemia (IDNA), ~16%, of premenopausal women (Cogswell et al., 2009). Changes in energy metabolism and
physical work capacity have been described in humans
and animals with iron depletion (Beard, 2001; Haas &
Brownlie, 2001; Willis, Brooks, Henderson, & Dallman,
1987). Compared with their sedentary counterparts,
female athletes are more susceptible to IDNA (2535%),
which is 57 times more prevalent than iron deficiency
with anemia (Constantini, Eliakim, Zigel, Yaaron, &
Falk, 2000; Dubnov & Constantini, 2004; Dubnov et al.,
2006; Malczewska, Blach, & Stupnicki, 2000; McClung,
Marchitelli, Friedl, & Young, 2006; Sinclair & Hinton,
2005). Beyond the age-related factor of menstrual status,
the increased prevalence of IDNA in active or training
women may be a result of one or a combination of the
following factors: hemolysis (foot strike, impact; Ehn,
Carlmark, & Hoglund, 1980; Peeling, Dawson, Goodman, Landers, & Trinder, 2008), increased iron loss
(gastrointestinal tract, hematuria, sweat; Weaver &
Rajaram, 1992), poor dietary iron intake (Fogelholm et
al., 1992; Hassapidou & Manstrantoni, 2001; McClung et
al., 2006; Steen, Mayer, Brownell, & Wadden, 1995), or
altered intestinal iron absorption, including the effects of
inflammation resulting from training (Akabas & Dolins,
2005; Beard & Tobin, 2000; Collins, Wessling-Resnick,
The authors are with the Div. of Nutritional Sciences, Cornell University, Ithaca, NY.

& Knutson, 2008; Peeling et al., 2008; Weight, Alexander, & Jacobs, 1991), although the exact mechanism is
unknown.
Collegiate rowers are endurance athletes who train
primarily at submaximal levels (7585% of their VO2max),
during which oxidative metabolism is the main energy
pathway and throughout which iron plays an important
role. It has been shown that the activity of iron-dependent enzymes and cytochromes needed for oxidative
metabolism are decreased in animals (Willis, Dallman,
& Brooks, 1988) and humans (Celsing, Ekblom, Sylven,
Everett, & Astrand, 1988) with IDNA, which leads to
impaired endurance performance. Thus, consequences
of IDNA particularly relevant to endurance athletes
include reduced endurance capacity and energetic efficiency (Hinton, Giordano, Brownlie, & Haas, 2000) and
increased local muscle fatigue (Brutsaert et al., 2003).
Serum ferritin (sFer) is the most common index
of body-iron stores and reflects iron stored in the liver.
sFer can be falsely elevated in an inflammatory state
(e.g., infection, postexercise), in which case inflammatory markers such as C-reactive protein or -1-acid
glycoprotein can aid in the assessment of iron status
(Beard, Murray-Kolb, Rosales, Solomons, & Angelilli,
2006; Northrop-Clewes, 2008; Thurnham et al., 2010).
Soluble transferrin receptor (sTfR), a transmembrane
protein regulated by cellular iron status, reflects iron
deficiency at the tissue level and is a more sensitive index
of functional iron deficiency than sFer. Unlike sFer, sTfR
is unaffected by inflammation and has been shown to
have lower within-subject variability in intensely training

501

502 DellaValle and Haas

athletes (Malczewska et al., 2000). sFer and sTfR respond


to iron supplementation in opposite directions (sTfR
decreases and sFer increases with supplementation or
repletion of iron stores). Total body iron (mg/kg) can be
calculated using a ratio of sTfR to sFer (Cook, Flowers, &
Skikne, 2003), but in a population with a low prevalence
of anemia, calculated total body iron is driven by sFer.
The purpose of this study was to examine the iron
status of female collegiate rowers at the beginning of a
training season and determine the association between
IDNA and reported rowing performance.

Methods
Recruitment of Subjects
This study was approved by the institutional review
boards of Cornell University, Binghamton University,
Syracuse University, Hobart & William Smith Colleges,
and Ithaca College. Rowers were recruited over a period
of 3 years (spring 2006, fall 2008, spring 2009, and fall
2009). Varsity and second-semester novice female rowers
who were >18 years of age and able to begin regular
training for their sport were eligible to participate in the
screening. Subjects were recruited at the beginning of the
conditioning phases of their competitive rowing seasons
(on arrival on campus postsummer and postwinter break).
Training activities during this time included general aerobic conditioning (cycling, running, rowing on ergometer),
resistance training, and high-intensity rowing training.
Team coaches were instrumental in recruitment and
screening efforts. A medical screening (NCAA-required)
before our screening excluded all athletes not healthy
enough to participate in their rowing training (current,
acute, or chronic illness; severe asthma; musculoskeletal problems). All rowers provided written voluntary
informed consent before participating in the study. Out
of 199 eligible female rowers, 165 completed the ironstatus screening. Subjects received iron-status results as
a benefit of participation, along with referral or recommendations to improve iron status if necessary.

Measurements
After NCAA medical clearance, iron-status variables
were measured for each subject and demographic, as
well as information on current dietary supplement use,
health and menstrual status, and habitual physical activity.
Height and weight were self-reported and later validated
with measured height and weight in a subsample of 48
subjects who participated in an intervention trial (height
r = .98, p < .001; weight r = .99, p < .001; no systematic bias). Time spent in light to moderate and vigorous
physical activity was quantified via self-report (habitual
endurance training and leisure-time physical activity
frequency, intensity, and duration; Craig et al., 2003).
Performance was assessed via self-reported best times
to complete a 2-km simulated race on the ergometer
from the previous season (23 months before iron-status

screening). Reported 2-km times were also later validated


with measured performance in the aforementioned subsample of 48 rowers (VO2peak, L/min: r = .69, p < .001;
4-km time, min: r = .64, p < .001).
Iron-status variables measured immediately after
nonfasting venous blood sampling (antecubital venipuncture into two evacuated tubes with EDTA and
serum separator) included hemoglobin, hematocrit, red
blood cell count (Beckman Coulter, Fullerton, CA),
sFer (Immulite 2000), sTfR (ELISA, Ramco Laboratories, Stafford, TX), and -1-acid glycoprotein (radial
immunodiffusion plate, Kent Laboratories, OR). Rowers
were classified as either iron depleted (sFer <20 g/L)
or normal (sFer 20 g/L). All anemic subjects (n = 16)
were notified of their status immediately after blood test
results (within 1 week of analysis) and referred to their
respective campus health services for further instruction
and monitoring or treatment.

Data Analysis
All data analysis was completed using SPSS (version
18.0, SPSS Inc., Chicago, IL). Data were examined to
verify normality of distribution, and skewed distributions
were log-transformed as appropriate. Descriptive statistics are presented as M SD. Students t test and ANOVA
were used to analyze differences between groups for
iron status (iron depleted vs. normal) with respect to all
variables measured. When a significant overall difference
was detected, Bonferronis post hoc analysis was used.
Pearsons correlations were used to examine associations
between variables. To investigate the effects of iron status
on physical performance, multiple-regression analysis
was conducted between physical performance (2-km
time) and sFer group status (based on sFer cutoff of 20.0
g/L) with potential confounders included as covariates
in the regression models (height, time spent training,
and years of rowing experience). A significance level
of p < .05 was used to test the main effect of iron status
on reported performance, and p < .10 was the level of
statistical significance used to test the interaction effects.

Results
Sixteen rowers (10%) were identified as anemic (hemoglobin <12.0 g/dl; Cogswell et al., 2009) and eliminated
from subsequent analyses. Results of the iron-status
screening of nonanemic rowers are presented in Table
1. Thirty percent (n = 44) of the nonanemic rowers were
found to be iron depleted (sFer <20.0 g/L), and 12% (n =
18) were clinically iron deficient (sFer <12.0 g/L). There
were no significant differences between rowers with
depleted or deficient iron status and those with normal
iron status in any demographic variable. Twenty-eight
nonanemic rowers (19%) had high values of sTfR (>8.0
mg/L; Brownlie, Utermohlen, Hinton, Giordano, & Haas,
2002), and 10% had total body iron <0 mg/kg, indicating severe iron deficiency. Three rowers had an -1-acid
glycoprotein value >140 mg/dl, indicating inflammation.

Effects of Iron Depletion on Female Athletes 503

Nineteen percent of screened subjects had a previous history of anemia or physician-diagnosed iron deficiency.
On average, rowers were 19.7 1.2 years of age and
170.7 7.3 cm tall and weighed 69.5 8.1 kg (BMI 23.7
3.3 kg/m2). Across the sample, rowers had 3.0 2.3

Table 1 Iron Status of Nonanemic Female


Collegiate Rowers (Between Schools) at the
Beginning of Training Season, N = 149
Iron-status index
Serum ferritin (g/L)

M SD
33.6 22.1

Log serum ferritin (g/L)

1.4 0.3

Hemoglobin (g/dl)

13.2 0.7

Red cell distribution width (%)

13.0 1.2

Hematocrit (%)

40.7 2.2

Mean cell volume (fl)

88.8 3.5

Soluble transferrin receptor (mg/L)

6.5 1.9

Total body iron (mg/kg)

3.8 3.0

Note. fl = femtoliter.

years rowing experience and a previous-season 2-km time


of 7 min and 48 s (469 25 s) and spent 6.4 2.2 hr/week
in combined moderate and vigorous physical activity.
Thirty-three percent of the sample reported consuming a
multivitamin/mineral supplement either intermittently or
regularly. Reported time spent in light to moderate physical activity per week was positively associated with years
of rowing experience (r = .29, p = .03), and height and
weight were negatively correlated with 2-km performance
time (r = .51 and .39, respectively, p < .001), with taller
and heavier rowers reporting faster times.
Multiple-regression analyses revealed that sFer
group, height, and years of rowing experience were
each a significant predictor of 2-km performance time
(p < .05). For these nonanemic subjects, hemoglobin
was not a significant predictor of 2-km time and was not
included in the multiple-regression models, and there
were no significant interactions between iron status and
the amount of time spent in physical activity. For rowers
with sFer <20.0 g/L, 2-km times were 21 s slower than
for rowers with normal iron status (p = .004; see Figure
1). As expected, the relationship between sFer status and
2-km time was stronger for those with sFer <15 g/L ( =
29.4 s, p = .002). This relationship remained significant

Figure 1 The impact of iron deficiency without anemia on rowers reported 2-km performance (means adjusted for years of
rowing experience and height, p = .004). *Depleted rowers (serum ferritin <20.0 g/L) significantly different from nondepleted
rowers (serum ferritin >20.0 g/L), p = .004.

504 DellaValle and Haas

using a higher sFer cutoff of 25 g/L ( = 17.4 s, p =


.01) but was no longer significant using a sFer cutoff of
30 g/L ( = 6.7 s, p = .38).

Discussion
The 30% prevalence of IDNA in the female rowers in this
study was similar to that previously reported for other
female athletes participating in endurance sports, as well
as female soldiers (Constantini et al., 2000; Dubnov &
Constantini, 2004; Dubnov et al., 2006; Malczewska et
al., 2000; McClung et al., 2006; Sinclair & Hinton, 2005).
It is possible that the prevalence of IDNA in our study
may have been affected by either chronic or intermittent
intake of multivitamin or mineral supplements, some
of which contain iron. Furthermore, the sFer cutoff of
20 g/L may have misclassified rowers as normal, and
examination of optimal sFer levels for female athletes
is warranted.
In addition to rowers physical characteristics, sFer
status was significantly related to reported 2-km performance times. We found a degree of association between
sFer status and reported performance times comparable
to what has been reported in iron-supplementation trials
(Brownlie et al., 2002; Brownlie, Utermohlen, Hinton, &
Haas, 2004; Brutsaert et al., 2003; Hinton et al., 2000),
confirming our sFer cutoff of 20 g/L as sensitive. Again,
using the cutoff of 20 g/L may have misclassified IDNA
rowers as normal, affecting this relationship. In this study,
42% of rowers had sFer <25 g/L, and the relationship
between sFer and reported 2-km performance time
remained significant using this cutoff.
It is biologically plausible that rowers 2-km time
is associated with poor iron status. As mentioned previously, there are several iron-dependent enzymes involved
in the transformation of chemical to mechanical energy
during oxidative metabolism, which is the main energy
pathway used by rowers during endurance training and
most competitive events performed submaximally, around
the lactate threshold. During high-intensity activities
such as a 2-km ergometer time trial, impaired O2 transport capacity, even in the absence of frank anemia, may
result in increased reliance on anaerobic metabolism to
produce energy (greater lactate production at an earlier
stage of exercise; Schoene et al., 1983; Zhu & Haas,
1998b). Because of the nature of this survey and our
self-reported performance variable, we did not have a
measure of maximal oxygen consumption or blood lactate
in these rowers, but this would be important to confirm
in the laboratory.
Our sample of collegiate female rowers is one at high
risk for iron depletion because of their menstrual status
and high training load, among other factors mentioned
herein. With the exception of the acute-phase protein
-1-acid glycoprotein as a marker of inflammation (which
was not used to exclude subjects from the analysis), these
factors were not measured in the current study.

Strategies to easily screen and improve iron status


may be useful for female endurance athletes at the beginning of a training season, because data suggest that iron
status of very active women may decrease with increased
levels of physical training over time (Ashenden, Martin,
Dobson, Mackintosh, & Hahn, 1998; Brigham, Beard,
Krimmel, & Kenney, 1993; Diehl, Lohman, Smith, &
Kertzer, 1986; McClung et al., 2009). In a recent study,
McClung et al. (2009) examined 94 female U.S. Army
recruits before and after 9 weeks of basic combat training
and found that sFer decreased by 20% (p < .01). In other
studies of female athletes, decreases in sFer (~25%) were
associated with training (Ashenden et al., 1998; Brigham
et al., 1993).
Early screening and iron supplementation, both of
which have been shown to improve resistance to fatigue
and endurance capacity in IDNA nonathletes (Brutsaert
et al., 2003; Hinton et al., 2000), may be beneficial to
female endurance athletes at the beginning of a season to
help prevent further decrements in iron status throughout
the training and competitive seasons. Given the modest
relationship between early-season iron status and recent
performance observed in this study, improving iron status
may improve endurance athletes adaptation to training,
as well as their performance in competition.
Not all potential confounders such as pre- and
postseason VO2peak and fat-free mass could be measured
in this cross-sectional study. As a result of logistic considerations of the current survey, a self-reported measure
of performance (2-km self-reported best time) during the
previous 23 months was used as an outcome. Although
the self-reported measure was highly correlated with
laboratory-derived values in a subsample of 48 rowers,
results should be interpreted with caution. The observed
association between IDNA and reported 2-km performance time is consistent with laboratory data showing
that IDNA impaired 15-km cycling time-trial performance in nonathletic women (Hinton et al., 2000; Zhu
& Haas, 1998a). It would be important to confirm these
results in a longitudinal study, preferably following the
same rowers periodically throughout both competitive
seasons of the academic year. Future research should
examine the dietary risk factors for IDNA, including
iron intake and bioavailability, as well as other markers
of iron metabolism, such as hepcidin.

Conclusions
Results from this study add to the evidence that iron status
is an important issue facing female endurance athletes at
the beginning of a training season. The prevalence of iron
depletion is higher in this population than in the general
population of young women because of many factors.
Female endurance athletes should be screened using a
sFer cutoff between 20.0 and 25.0 g/L to identify iron
depletion, which is likely to impair performance. Athletes with a history of anemia or iron deficiency should

Effects of Iron Depletion on Female Athletes 505

receive counseling regarding supplementation and food


choices, as well as serial monitoring of their iron status
(hemoglobin, sFer).
Acknowledgments
This research was funded by grants from the American Dietetic
Association Foundation (Jean Hankin Nutritional Epidemiology Research Grant) and Cornell Universitys Division of
Nutritional Sciences.

References
Akabas, S.R., & Dolins, K.R. (2005). Micronutrient requirements of physically active women: What can we learn
from iron? The American Journal of Clinical Nutrition,
81(5), 1246S1251S.
Ashenden, M., Martin, D., Dobson, G., Mackintosh, C., &
Hahn, A. (1998). Serum ferritin and anemia in trained
female athletes. International Journal of Sport Nutrition,
8(3), 223229.
Beard, J., & Tobin, B. (2000). Iron status and exercise. The
American Journal of Clinical Nutrition, 72(2), 594S597S.
Beard, J.L. (2001). Iron biology in immune function, muscle
metabolism and neuronal functioning. The Journal of
Nutrition, 131(2S-2), 568S580S.
Beard, J.L., Murray-Kolb, L.E., Rosales, F.J., Solomons, N.W.,
& Angelilli, M.L. (2006). Interpretation of serum ferritin
concentrations as indicators of total-body iron stores in
survey populations: The role of biomarkers for the acute
phase response. The American Journal of Clinical Nutrition, 84(6), 14981505.
Brigham, D., Beard, J., Krimmel, R., & Kenney, W. (1993).
Changes in iron status during competitive season in female
collegiate swimmers. Nutrition, 9(5), 418422.
Brownlie, T., IV, Utermohlen, V., Hinton, P.S., Giordano, C.,
& Haas, J.D. (2002). Marginal iron deficiency without
anemia impairs aerobic adaptation among previously
untrained women. The American Journal of Clinical
Nutrition, 75(4), 734742.
Brownlie, T., IV, Utermohlen, V., Hinton, P.S., & Haas, J.D.
(2004). Tissue iron deficiency without anemia impairs
adaptation in endurance capacity after aerobic training
in previously untrained women. The American Journal
of Clinical Nutrition, 79(3), 437443.Brutsaert, T.D.,
Hernandez-Cordero, S., Rivera, J., Viola, T., Hughes,
G., & Haas, J.D. (2003). Iron supplementation improves
progressive fatigue resistance during dynamic knee extensor exercise in iron-depleted, nonanemic women. The
American Journal of Clinical Nutrition, 77(2), 441448.
Celsing, F., Ekblom, B., Sylven, C., Everett, J., & Astrand,
P. (1988). Effects of chronic iron deficiency anaemia on
myoglobin content, enzyme activity, and capillary density
in the human skeletal muscle. Acta Medica Scandinavica,
223(5), 451457.
Cogswell, M.E., Looker, A.C., Pfeiffer, C.M., Cook, J.D.,
Lacher, D.A., Beard, J.L., . . . Grummer-Strawn, L.M.
(2009). Assessment of iron deficiency in US preschool
children and nonpregnant females of childbearing
age: National health and nutrition examination survey
20032006. The American Journal of Clinical Nutrition,
89(5), 13341342.

Collins, J.F., Wessling-Resnick, M., & Knutson, M.D. (2008).


Hepcidin regulation of iron transport. The Journal of
Nutrition, 138(11), 22842288.
Constantini, N., Eliakim, A., Zigel, L., Yaaron, M., & Falk,
B. (2000). Iron status of highly active adolescents: Evidence of depleted iron stores in gymnasts. International
Journal of Sport Nutrition and Exercise Metabolism,
10(1), 6270.
Cook, J.D., Flowers, C.H., & Skikne, B.S. (2003). The quantitative assessment of body iron. Blood, 101(9), 33593364.
Craig, C., Marshall, A., Sjostrom, M., Bauman, A., Booth, M.,
Ainsworth, B., . . . Oja, P. (2003). International physical
activity questionnaire: 12-country reliability and validity. Medicine and Science in Sports and Exercise, 35(8),
13811395.
Diehl, D., Lohman, T., Smith, S., & Kertzer, R. (1986). Effects
of physical training and competition on the iron status
of female field hockey players. International Journal of
Sports Medicine, 7(5), 264270.
Dubnov, G., & Constantini, N. (2004). Prevalence of iron
depletion and anemia in top-level basketball players.
International Journal of Sport Nutrition and Exercise
Metabolism, 14(1), 3037.
Dubnov, G., Foldes, A., Mann, G., Magazanik, A., Siderer,
M., & Constantini, N. (2006). High prevalence of iron
deficiency and anemia in female military recruits. Military
Medicine, 171(9), 866869.
Ehn, L., Carlmark, B., & Hoglund, S. (1980). Iron status in
athletes involved in intense physical activity. Medicine and
Science in Sports and Exercise, 12(1), 6164.
Fogelholm, M., Rehunen, S., Gref, C., Laakso, J., Lehto, J.,
Ruokonen, I., & Himberg, J.J. (1992). Dietary intake and
thiamin, iron, and zinc status in elite Nordic skiers during
different training periods. International Journal of Sport
Nutrition, 2(4), 351365.
Haas, J.D., & Brownlie, T., IV. (2001). Iron deficiency and
reduced work capacity: A critical review of the research to
determine a causal relationship. The Journal of Nutrition,
131(2S-2), 676S690S.
Hassapidou, M., & Manstrantoni, A. (2001). Dietary intakes of
elite female athletes in Greece. Journal of Human Nutrition
and Dietetics, 14(5), 391396.
Hinton, P.S., Giordano, C., Brownlie, T., & Haas, J.D. (2000).
Iron supplementation improves endurance after training
in iron-depleted, nonanemic women. Journal of Applied
Physiology, 88(3), 11031111.
Malczewska, J., Blach, W., & Stupnicki, R. (2000). The effects
of physical exercise on the concentrations of ferritin and
transferrin receptor in plasma of female judoists. International Journal of Sport Medicine, 21(3), 175179.
McClung, J., Karl, J., Cable, S., Williams, K., Young, A., &
Lieberman, H. (2009). Longitudinal decrements in iron
status during military training in female soldiers. British
Journal of Nutrition,102(4), 605609.
McClung, J.P., Marchitelli, L.J., Friedl, K.E., & Young, A.J.
(2006). Prevalence of iron deficiency and iron deficiency
anemia among three populations of female military personnel in the US army. Journal of the American College
of Nutrition, 25(1), 6469.
Northrop-Clewes, C.A. (2008). Interpreting indicators of iron
status during an acute phase responseLessons from
malaria and human immunodeficiency virus. Annals of
Clinical Biochemistry, 45(Pt. 1), 1832.

506 DellaValle and Haas

Peeling, P., Dawson, B., Goodman, C., Landers, G., & Trinder,
D. (2008). Athletic induced iron deficiency: New insights
into the role of inflammation, cytokines and hormones.
European Journal of Applied Physiology, 103(4), 381391.
Schoene, R., Escourrou, P., Robertson, H., Nilson, K., Parsons,
J., & Smith, N. (1983). Iron repletion decreases maximal
exercise lactate concentrations in female athletes with
minimal iron-deficiency anemia. Journal of Laboratory
and Clinical Medicine, 102(2), 306312.
Sinclair, L., & Hinton, P. (2005). Prevalence of iron deficiency
with and without anemia in recreationally active men and
women. Journal of the American Dietetic Association,
105(6), 975978.
Steen, S., Mayer, K., Brownell, K., & Wadden, T. (1995).
Dietary intake of female collegiate heavyweight rowers.
International Journal of Sport Nutrition, 5(3), 225231.
Thurnham, D.I., McCabe, L.D., Haldar, S., Wieringa, F.T.,
Northrop-Clewes, C.A., & McCabe, G.P. (2010). Adjusting plasma ferritin concentrations to remove the effects
of subclinical inflammation in the assessment of iron
deficiency: A meta-analysis. The American Journal of
Clinical Nutrition, 92(3), 546555.

Weaver, C. M., & Rajaram, S. (1992). Exercise and iron status.


The Journal of Nutrition, 122(3 Suppl.), 782787.
Weight, L., Alexander, D., & Jacobs, P. (1991). Strenuous
exercise: Analogous to the acute-phase response? Clinical
Science (Lond), 81(5), 677683.
Willis, W.T., Brooks, G.A., Henderson, S.A., & Dallman, P.R.
(1987). Effects of iron deficiency and training on mitochondrial enzymes in skeletal muscle. Journal of Applied
Physiology, 62(6), 24422446.
Willis, W.T., Dallman, P.R., & Brooks, G.A. (1988). Physiological and biochemical correlates of increased work in
trained iron-deficient rats. Journal of Applied Physiology,
65(1), 256263.
Zhu, Y.I., & Haas, J.D. (1998a). Altered metabolic response
of iron-depleted nonanemic women during a 15-km time
trial. Journal of Applied Physiology, 84(5), 17681775.
Zhu, Y.I., & Haas, J.D. (1998b). Response of serum transferrin
receptor to iron supplementation in iron-depleted, nonanemic women. The American Journal of Clinical Nutrition,
67(2), 271275.

You might also like