Secondary Logo

Journal Logo

Hematological indices and iron status in athletes of various sports and performances

OLAF SCHUMACHER, YORCK; SCHMID, ANDREAS; GRATHWOHL, DOMINIK; BÜLTERMANN, DIRK; BERG, ALOYS

Medicine & Science in Sports & Exercise: May 2002 - Volume 34 - Issue 5 - p 869-875
APPLIED SCIENCES: Physical Fitness and Performance
Free

SCHUMACHER, Y. O., A. SCHMID, D. GRATHWOHL, D. BÜLTERMANN, and A. BERG. Hematological indices and iron status in athletes of various sports and performances. Med. Sci. Sports Exerc., Vol. 34, No. 5, pp. 869–875, 2002.

Purpose Alterations of the red blood cell system and iron metabolism can influence physical performance. On the other hand, exercise can influence hematological variables. The purpose of this epidemiological study was to investigate the characteristics of the red blood cell system and the iron metabolism in athletes of different sporting disciplines and at different levels of performance.

Methods We studied 851 male subjects (747 athletes, 104 untrained controls). Hemoglobin (Hb), hematocrit (Hct), red blood cell count (RBC), iron, transferrin, ferritin (Fer), and haptoglobin were analyzed in standardized blood samples, obtained after 2 d of rest, considering levels of performance (internationally, nationally, locally competitive, and leisure time), distinctive sporting category (endurance- (END), strength- (POW), and mixed-trained (MIX)), and, within endurance athletes, distinctive disciplines (cycling (CYC) and running (RUN)).

Results No difference was found between athletes and controls in Hb and Hct. Reduced Hb, Hct, and RBC levels were observed in END compared with POW and MIX. These findings can mainly be attributed to exercise-induced plasma volume expansion, and only to a lesser degree and in selected athlete populations to hemolysis, as low haptoglobin is only observed in RUN, not in CYC, suggesting that not exercise itself but the “traumatic” movement of running might trigger the destruction of red blood cells. Physical activity of increasing duration and workloads (leisure time compared with competitive athletes) leads to decreased Fer levels in athletes, disregarding their discipline, but more pronounced in RUN.

Conclusion Physical training itself has no significant effect on selected hematological variables in athletes compared with untrained controls. The specific type and duration of exercise is of major importance in the adaptations of the blood cell system and the iron metabolism.

Department of Prevention, Rehabilitation and Sports Medicine, University of Freiburg, GERMANY

Submitted for publication May 2001.

Accepted for publication September 2001.

Alterations of the red blood cell system are known to considerably influence physical performance: anemia has negative effects on physical exercise capacity. An increase in red blood cell mass was shown to enhance aerobic performance. On the other hand, exercise can influence hematological variables: numerous investigations reported the adaptations of blood and iron variables to endurance exercise (5,23): hematocrit (Hct), hemoglobin concentration (Hb), and red blood cell count (RBC) are reduced in endurance-trained athletes, mainly due to exercise-induced plasma volume (PV) expansion, which sets in within a few days of prolonged training. Nevertheless, the absolute Hb mass is increased, as exercise stimulates erythrocytosis, but this mechanism is outpaced by the far greater increase in PV: PV adaptation is mediated by a higher fluid retention in the body, resulting in lower Hct and Hb readings in endurance athletes (22). A higher PV can increase exercise capacity through an increased cardiac output and by reducing blood viscosity, thereby optimizing microcirculation and improving oxygen delivery to the working muscle. Other authors described exercise induced destruction of red blood cells to contribute to a lesser degree to lower Hb and Hct in endurance athletes through the so-called “foot-strike hemolysis” (8,14).

Iron plays a key role in number of cellular processes, such as DNA synthesis and electron transport. Furthermore, it is an essential element of Hb, the blood’s oxygen carrier. By these means, iron depletion can affect physical performance. Iron depletion is a common trace mineral disorder in athletes, as exercise was reported to result in a higher iron turnover (4). Nowadays, ferritin is used as the most common indicator of iron status.

Although many authors describe the influence of various types of exercise on hematological variables and iron metabolism, data comparing these variables in different sports as well as within different levels of performance in distinctive sporting disciplines are scarce. In addition, hematological indices and variables of the iron metabolism have been included in several indirect models for the detection of erythropoietin-abuse in athletes (19) and research evaluating these variables and their reaction to exercise needs to be completed in order to further improve these tests. Therefore, the purpose of this epidemiological study was to investigate the characteristics of the red blood cell system and iron metabolism in athletes at different levels of performance and in distinctive sporting disciplines.

Back to Top | Article Outline

MATERIALS AND METHODS

Subjects.

A total of 851 male subjects attending routine health checks including a laboratory investigation and exercise testing at our department gave their written informed consent to participate in the study, which was approved by the ethic commission of our institution. All participants completed a questionnaire assessing their physical activity, sporting discipline, and weekly training workload. Subjects with pathological findings during physical examination or laboratory testing, recent history of disease, altitude exposure, or intake of iron supplements or other medications were excluded. The subjects followed a normal, balanced Western diet. Vegetarians were excluded. Two days before the investigation, the subjects withstood from strenuous physical training.

Back to Top | Article Outline

Questionnaire.

The questionnaire investigated the sporting category and specific discipline, the weekly amount of training (hours), and the level of physical performance (nonactive/sedentary, leisure-time athletes, locally competitive, nationally competitive, or internationally competitive) of every participant.

Based on this information, the subjects were then divided into two different main groups: athletes (ATH) and sedentaries (SED). The group of athletes was subdivided according to the respective main disciplines into three categories: endurance athletes (END) (subjects practicing endurance sports, such as cycling, running, or other endurance sports); strength-trained athletes (POW) (weight lifting, wrestling, shot-put, hammer-throwing, javelin, or discus); and mixed athletes (MIX) (soccer, volleyball, basketball, ice-hockey, handball, tennis, table tennis, or badminton). Within the categories of endurance and power athletes, the subjects were finally sorted by their level of performance (leisure-time athletes (LT), locally competitive (LC), nationally competitive (NC), or internationally competitive (IC)). Subjects not clearly fitting in one of these categories were excluded.

Back to Top | Article Outline

Laboratory investigations.

Blood sampling took place under standardized conditions in supine position on an empty stomach in the morning. Blood was drawn from a cubital vein into a 4-mL K-EDTA coated Vacutainer system and a 9 mL Vacutainer system containing beads for serum separation (S-Monovette KE, Sarstedt, Nürnbrecht, Germany). In the EDTA samples, the following variables were analyzed by an automated cell counter (Serono-Baker Diagnostics, Allentown, PA; Model 9000 Diff) within 3 h of the prelevation: Hb (g·dL−1), Hct (%), and red blood cell count (106·mm−3). After centrifugation of the serum sample, the following variables were determined: iron (kit: Dade Behring; analyzer: Dade Behring BNA 1000, Dade Behring, Marburg, Germany); ferritin (Boehringer Mannheim Immundiagnostica, Mannheim, Germany); and haptoglobin and transferrin (kit: Roche Diagnostics; Analyzer: Roche/Hitachi Modular, Roche Diagnostics, Mannheim, Germany).

Back to Top | Article Outline

Exercise testing.

Every subject was submitted to an incremental running or cycling test until volitional exhaustion to evaluate physical performance: cycle-ergometry testing on an electronically braked ergometer (Lode Excalibur, Lode, Groningen, The Netherlands) started at 100 W with a 50-W increase every 3 min. The subjects were instructed to maintain a cadence of 85–95 rpm. Initial running speed on a treadmill (Woodway XELG 2, Woodway, Weil am Rhein, Germany) was set at 8 km·h−1 and was increased by 2 km·h−1 every 3 min. Oxygen uptake (O2) was measured using an automated breath-by-breath analyzing system (Oxycon, Jaeger GmbH, Frankfurt, Germany). The highest O2 measured during the last stage of exercise performed before exhaustion was considered as peak oxygen uptake (O2peak). Additionally, the oxygen uptake-power output (cycling) or speed (running) relationship was considered, to see if there was a plateau.

Height and body weight were measured; body mass index (BMI) was calculated as body weight (kg)/(height (m))2. The anthropometric and physiological characteristics of the participants are shown in Table 1.

Table 1

Table 1

Back to Top | Article Outline

Statistical analysis.

Statistical analysis was performed using the Statistical Package for Social Sciences (SPSS for Windows, Version 10.0, SPSS Inc., Chicago IL). Data were checked for normal distribution using the Kolmogorov-Smirnov test, normally distributed variables are presented as mean values ± SD, not normally distributed data as median and range. The Mann-Whitney U-test for independent samples was used for the calculation of group differences. P-values < 0.05 were regarded as statistically significant.

Back to Top | Article Outline

RESULTS

Anthropometric and physiological data.

The analyzed groups differed in their age, body weight, training habits, and O2peak. Compared with sedentaries, athletes showed lower body weight, lower age, higher training workload, and higher O2peak. Within the group of athletes (LT, LC, NC, and IC) significant differences in O2peak and training workload were observed. Considering the different sporting categories, endurance-trained athletes, especially runners, showed lower body weight and BMI, and higher O2peak when compared with strength- and mixed-trained athletes. Within the endurance-trained athletes, no significant difference in BMI was observed. The results are summarized in Table 1.

Back to Top | Article Outline

Hematological data.

Compared with sedentaries, athletes showed higher RBC with no significant difference in Hb or Hct. Within the athlete population, higher readings for Hb, Hct, and RBC were found in strength-trained athletes when compared with endurance- or mixed-trained subjects. Considering the level of performance, analysis revealed lower RBC and Hb values for leisure-time athletes when compared with competitive sportsmen. Furthermore, nationally competitive athletes displayed higher hematological indices than their internationally competitive counterparts. Except a lower Hct in nationally competitive compared with leisure time strength-trained athletes, these performance-level–related changes in hematological variables were only observed in the endurance category. Tables 2 and 3 show the hematological data of the studied groups.

Table 2

Table 2

Table 3

Table 3

Back to Top | Article Outline

Iron metabolism.

Serum iron did not show any significant difference between athletes and sedentaries. Within endurance-trained athletes, cyclists showed higher iron readings than runners. The type of sport seems not to influence iron levels in the studied group, as strength-, endurance-, and mix-trained athletes displayed no significant group-differences. In contrast, international and national competitors in strength and endurance events showed a higher serum iron concentration than the locally competitive athletes.

Athletes displayed significantly lower ferritin values than sedentaries. No significant difference was found between the different sporting categories (END, MIX, and POW). When analyzing endurance athletes, runners showed lower ferritin readings than cyclists. Considering the level of performance, leisure time athletes presented higher ferritin than competitive strength- and endurance-trained athletes.

Transferrin showed no significant difference between trained and untrained subjects. Contrasting ferritin, transferrin presented higher readings in runners compared with cyclists. Considering the level of performance, internationally competitive athletes showed the lowest transferrin concentrations in endurance-trained athletes.

Haptoglobin showed no significant difference between athletes and nonathletes; neither the different sporting categories nor the different levels of performance displayed any significant difference in this variable. When considering specific disciplines, runners showed significantly lower haptoglobin concentrations compared to cyclists.

The iron-related variables are summarized in Tables 3 and 4.

Table 4

Table 4

Back to Top | Article Outline

DISCUSSION

Athletes versus sedentary persons.

The influence of physical activity on hematological variables has been studied under many purposes. Although several authors demonstrated decreased Hb, Hct, and RBC in athletes disregarding their sporting discipline compared with physically inactive controls, others argue that these changes are not mainly depending on physical activity itself but on the specific type of exercise, such as endurance training (11,12,20,26). Our data from a large number of male athletes of various sports support these findings, as no difference between Hb and Hct levels in inactive controls and our collective of physically active subjects in general was found. Nevertheless, it has to pointed out that acute hemodiluting effects of exercise are not considered in the present study, as blood sampling was performed after 2 d of reduced sporting activity and the moment of sampling was not standardized with respect to the individual seasonal training and competition schedule of the tested athletes (9).

Female athletes were not considered in the present study, as they are not only submitted to exercise- or diet-related changes in their blood and iron metabolism, but the monthly blood loss through menstruation might lead to a further decrease in the related variables, such as Hb, Hct iron, and ferritin. Furthermore, it is known that amenorrhoea and oligomenorrhea are frequent in female athletes. The incidence of these conditions varies strongly, depending on the type of sport and the amount of training, making a comparison of performance- and training-related changes in the blood cell system and the iron metabolism difficult in the female athlete population. Nevertheless, other investigations have shown that when compared with power-trained and sedentary female subjects, endurance-trained women showed lower Hb, Hct, and ferritin (13).

Iron and especially ferritin, the iron storage protein, has been demonstrated to be reduced in athletes, due to higher iron turnover and increased synthesis of iron-containing proteins paired with altered intestinal absorption and an increased loss through sweat, the intestines, and kidneys (15,18). Our data underline these findings for athletes, as their ferritin presents significantly reduced compared to sedentary persons. Nevertheless, the ferritin levels of the examined athletes are still well within the normal range, suggesting that any impairment of metabolic functions due to exercise induced iron shortage is rather unlikely. Exercise-induced hemolysis, often addressed to be a reason for reduced iron and ferritin levels or even anemias in athletes seems to be of no role in the reduced ferritin levels in the general population of our athletes, as haptoglobin shows no significant difference to physically inactive subjects. Thus, this mechanism might play a role in selected populations of athletes.

Back to Top | Article Outline

Sporting categories.

Most reports describing hematological changes induced by sporting activity focus on specific disciplines or special training characteristics, such as endurance or strength training. The effects of endurance sports have been extensively studied: hematological changes reported for endurance-trained athletes when compared with the normal population include decreased Hb, Hct, and RBC, associated with reticulocytosis or an increased number of young erythrocytes, characterized by lower corpuscular Hb content and a higher cell volume (3,10,26,27). Our data support these findings for endurance-trained athletes, not only when compared with sedentaries but also in comparison with strength-trained athletes. Mixed-trained athletes show a trend toward lower variables compared with strength-trained sportsmen. The mechanisms leading to these adaptations have been widely investigated and discussed: endurance exercise induces plasma volume expansion, mediated by increased production of aldosterone and osmotically active plasma proteins and a decreased urodilatin activity and sensibility of central baroreceptors situated in the medulla oblongata, one of the body’s mechanisms to register and adjust intravascular volume. These adjustments result in a higher fluid retention in the body and consecutively lower Hct and Hb readings (6,28). The adaptations set in within a few days of prolonged training. In addition, the absolute Hb mass is increased, as exercise stimulates erythrocytosis. Nevertheless, the Hb increase is outpaced by the far greater increase in plasma volume, resulting in lower RBC, Hb, and Hct. The increased plasma volume is aimed to compensate for the negative effects of acute exercise induced hemoconcentration (fluid loss through increased capillary permeability, higher osmotic pressure in the working muscle, and sweating) (22). A higher plasma volume can increase exercise capacity through an increased cardiac output and by reducing blood viscosity, thereby optimizing microcirculation and improving oxygen delivery to the working muscle as well as thermoregulation. This physiological hemodilution has often been addressed as “sports pseudoanemia” (27).

In contrast to other investigations, where one type of endurance sport (mostly running) is compared to strength sports or the normal population, our investigation with an analysis of various sporting categories and a wide range of disciplines did not show any significant difference in haptoglobin or iron related variables within the different sporting categories (END, MIX, and POW). These findings suggest that endurance training itself, despite the high training workload, does not lead to an increased hemolysis or higher iron requirement when compared with strength- or mixed-training.

Back to Top | Article Outline

Endurance sport disciplines.

As stated, endurance-trained athletes display decreased Hb, Hct, and RBC values. It has been demonstrated that these variables are highly sensible to acute effects of exercise and display seasonal adaptations, depending on training and competition schedule of the studied athletes (24). These conditions were not considered in the present investigation. In our data, no significant difference between runners and cyclists was found for Hb and RBC.

Haptoglobin has been reported to be decreased in endurance runners, indicating a marked hemolysis in these athletes (7,16). This has been attributed to increased turnover of red blood cells with accelerated destruction of these cells by different exercise-related mechanisms, such as squeezing and rupture of erythrocytes by treading on the foot-sole (so-called “foot-strike hemolysis”), during muscle contraction in capillaries, by increased renal blood flow and blood pressure paired with impaired glomerular permeability, increased body temperature, or acute, exercise-induced acidosis. Several investigations support the high erythrocyte turnover by demonstrating a shift in the erythroid blood profile of endurance-trained athletes toward younger cells with higher mean corpuscular volume. In addition, hematuria and hemoglobinuria have not only been observed in long-distance runners but also in triathletes, swimmers, and after strength-training programs (1,12,25). In accordance with these findings, our data report a significantly decreased haptoglobin in runners. The haptoglobin levels in this group were partly situated below the normal range for healthy subjects. Despite their high training workload, cyclists did not show any significant differences in haptoglobin levels compared with untrained controls. These data support the aforementioned argument that not the endurance exercise itself but mainly its mechanical, traumatic component during running exercise triggers the accelerated hemolysis. It has to be noticed that our investigation was carried out after 2 d of relative rest and that short-term hemolytic effects of exercise might not be visible in our data.

In accordance with other reports, iron and ferritin levels were found to be reduced in runners when compared with cyclists. These findings can be attributed to increased hemolysis and higher iron turnover through the so-called “foot-strike hemolysis” in this discipline requiring a higher iron turnover. These facts do not necessarily represent a general sign of iron depletion, as after intravasal hemolysis, iron might be recycled via haptoglobin-Hb complexes through the hepatocytes in the liver, thus bypassing ferritin: Magnusson et al. (17) found replenished iron stores in the bone marrow of runners with reduced ferritin levels. Nevertheless, it has to be pointed out that in the absence of hypothyroidism or vitamin C deficiency, serum ferritin directly reflects the body iron stores.

The loss of iron through sweating or reduced iron intake due to specific diets are other possible causes for reduced iron levels and ferritin stores. For the examined group of endurance-trained athletes, these issues seem unlikely to be responsible for the difference between runners and cyclists, as athletes following specific diets or vegetarians were excluded from the investigation and body composition, a major issue in both running and cycling, is comparable in our athletes as represented by similar BMI in all endurance-trained groups. Furthermore, it can be assumed that iron loss through sweat is comparable in runners and cyclists, as they all perform high amounts of weekly training. Nevertheless, iron and ferritin readings are markedly reduced in our population of runners with high training workload and should be controlled on a regular base to prevent iron depletion. Contrasting this, cyclists do not show any signs of increased hemolysis and a higher iron requirement. Therefore, the prophylactic iron substitution often practiced in competitive cycling cannot be justified from a medical point of view.

Back to Top | Article Outline

Training workload and level of performance.

The influence of different training intensities and levels of performance on variables of the hematological system have not been studied to a great extend. Allen et al. (2) reported the well-known pseudoanemia as a result of moderate endurance training, which, with ongoing training, was accompanied by indices of hemolysis and shifts toward younger cells in the blood profile. Nevertheless, these adaptations occur only after a certain time of endurance training and are connected with an increased red cell mass. For brief exercise duration and low-intensity training programs, the red cell mass remains constant, and only short-term shifts in plasma volume are observed (22). Our data from athletes support these findings: endurance-trained leisure time athletes with training workloads around 3 h·wk−1 display significantly lower Hb and RBC compared with all other groups of endurance-trained sportsmen. Endurance-trained competitive athletes show, with increasing amount of weekly training, an increase in Hb and RBC. Although these findings might seem contradictory to the aforementioned adaptations with decreased Hb, Hct, and RBC in endurance-trained athletes, it has to be mentioned that the hemodilutive effects of exercise with expanded plasma volume might be of reduced significance in our population, as testing took place after 2 d of rest and plasma volume expansion might have partially resolved. Nevertheless, a misuse of recombinant human erythropoietin to boost erythropoiesis, and thereby Hb and Hct, cannot be completely excluded in the studied athletes but seems rather unlikely to affect the collective on a larger scale, as all athletes were under close medical monitoring. Different workloads of strength training had no significant influence on the measured hematological variables.

Red cell mass and total Hb mass, but not Hb concentration, have been reported to be directly related to oxygen uptake. In our data, no connection between the hematological variables and O2peak could be established. This adds to the argument, that hematological concentrations (Hb, Hct), as measured in most studies, are of limited use. For this reason, it seems necessary to consider absolute values, such as red cell mass, total Hb mass, or plasma volume, to accurately describe changes within the blood cell variables (21).

No significant difference between haptoglobin and the influence of different levels of performance and training workloads on this variable was found. Despite this fact, strength- and endurance-trained athletes with training workloads over 5.8 h·wk−1 showed lower variables of the iron metabolism, suggesting that in addition to the exercise induced hemolysis of runners, a higher iron turnover might be visible in these athletes. Analysis of other iron related variables, such as soluble transferrin receptor (sTfr), could further clarify these findings.

Back to Top | Article Outline

CONCLUSION

In this epidemiological study with a high number of subjects, we find that physical training itself has no decreasing effect on selected hematological variables in athletes but that the type of physical exercise plays a major role. Reduced Hb, Hct, and RBC levels observed in endurance-trained athletes, so-called “athletes pseudoanemia” can mainly be attributed to an exercise-induced plasma volume expansion and only to a lesser degree and in selected athlete populations to hemolysis. In this study, indices of exercise-associated hemolytic processes with low haptoglobin are only observed in endurance runners, not in cyclists, suggesting that not exercise itself but the “traumatic” movement of running triggers the destruction of the red blood cells (“foot-strike hemolysis”). Physical activity leads to decreased ferritin levels in athletes regardless of their discipline, but they are more pronounced in runners. For these reasons, the iron metabolism of athletes, especially those of runners, should be closely monitored to avoid depletion and initiate substitutive therapy whenever necessary.

Address for correspondence: Yorck Olaf Schumacher, M.D., Abteilung Rehabilitation, Prävention und Sportmedizinm, Medizinische Universitätsklinik Freiburg, Hugstetter Str. 55, 79106 Freiburg, Germany; E-mail: olaf@msm1.ukl.uni-freiburg.de.

Back to Top | Article Outline

REFERENCES

1. Abarbanel, J., A. E. Benet, D. Lask, and D. Kimche. Sports hematuria. J. Urol. 143: 887–890, 1990.
2. Allen, M. E., B. S. Tully, and A. M. Bieling. Plasma volume expansion following mild aerobic exercise. Sports Med. Train. Rehabil. 3: 157–163, 1992.
3. Casoni, I., C. Borsetto, A. Cavicchi, S. Martinelli, and F. Conconi. Reduced hemoglobin concentration and red cell hemoglobinization in Italian marathon and ultramarathon runners. Int. J. Sports Med. 6: 176–179, 1985.
4. Clarkson, P. M., and E. M. Haymes. Exercise and mineral status of athletes: calcium, magnesium, phosphorus, and iron. Med. Sci. Sports Exerc. 27: 831–843, 1995.
5. Convertino, V. A. Blood volume: its adaptation to endurance training. Med. Sci. Sports Exerc. 23: 1338–1348, 1991.
6. Convertino, V. A., P. J. Brock, L. C. Keil, E. M. Bernauer, and J. E. Greenleaf. Exercise training-induced hypervolemia: role of plasma albumin, renin, and vasopressin. J. Appl. Physiol. Respir. Environ. Exerc. Physiol. 48: 665–669, 1980.
7. Dufaux, B., A. Hoederath, I. Streitberger, W. Hollmann, and G. Assmann. Serum ferritin, transferrin, haptoglobin, and iron in middle- and long-distance runners, elite rowers, and professional racing cyclists. Int. J. Sports Med. 2: 43–46, 1981.
8. Eichner, E. R. Runner’s macrocytosis: a clue to footstrike hemolysis: runner’s anemia as a benefit versus runner’s hemolysis as a detriment. Am. J. Med. 78: 321–325, 1985.
9. Fellmann, N. Hormonal and plasma volume alterations following endurance exercise: a brief review. Sports Med. 13: 37–49, 1992.
10. Green, H. J., G. Coates, J. R. Sutton, and S. Jones. Early adaptations in gas exchange, cardiac function and haematology to prolonged exercise training in man. Eur. J. Appl. Physiol. Occup. Physiol. 63: 17–23, 1991.
11. Green, H. J., J. R. Sutton, G. Coates, M. Ali, and S. Jones. Response of red cell and plasma volume to prolonged training in humans. J. Appl. Physiol. 70: 1810–1815, 1991.
12. Guglielmini, C., I. Casoni, M. Patracchini, et al. Reduction of hemoglobin levels during the racing season in nonsideropenic professional cyclists. Int. J. Sports Med. 10: 352–356, 1989.
13. Haymes, E. M., and D. M. Spillman. Iron status of women distance runners, sprinters, and control women. Int. J. Sports Med. 10: 430–433, 1989.
14. Hunding, A., R. Jordal, and P. E. Paulev. Runner’s anemia and iron deficiency. Acta Med. Scand. 209: 315–318, 1981.
15. Lampe, J. W., J. L. Slavin, and F. S. Apple. Poor iron status of women runners training for a marathon. Int. J. Sports Med. 7: 111–114, 1986.
16. Magnusson, B., L. Hallberg, L. Rossander, and B. Swolin. Iron metabolism and “sports anemia.” I. A study of several iron parameters in elite runners with differences in iron status. Acta Med. Scand. 216: 149–155, 1984.
17. Magnusson, B., L. Hallberg, L. Rossander, and B. Swolin. Iron metabolism and “sports anemia.” II. A hematological comparison of elite runners and control subjects. Acta Med. Scand. 216: 157–164, 1984.
18. Newhouse, I. J., and D. B. Clement. Iron status in athletes: an update. Sports Med. 5: 337–352, 1988.
19. Parisotto, R., C. J. Gore, K. R. Emslie, et al. A novel method utilising markers of altered erythropoiesis for the detection of recombinant human erythropoietin abuse in athletes. Haematologica 85: 564–572, 2000.
20. Sawka, M. N., V. A. Convertino, E. R. Eichner, S. M. Schnieder, and A. J. Young. Blood volume: importance and adaptations to exercise training, environmental stresses, and trauma/sickness. Med. Sci. Sports Exerc. 32: 332–348, 2000.
21. Schmidt, W., B. Biermann, P. Winchenbach, S. Lison, and D. Boning. How valid is the determination of hematocrit values to detect blood manipulations? Int. J. Sports Med. 21: 133–138, 2000.
22. Schmidt, W., N. Maassen, U. Tegtbur, and K. M. Braumann. Changes in plasma volume and red cell formation after a marathon competition. Eur. J. Appl. Physiol. Occup. Physiol. 58: 453–458, 1989.
23. Schmidt, W., N. Maassen, F. Trost, and D. Boning. Training induced effects on blood volume, erythrocyte turnover and haemoglobin oxygen binding properties. Eur. J. Appl. Physiol. Occup. Physiol. 57: 490–498, 1988.
24. Schumacher, Y. O., D. Grathwohl, J. M. Barturen, et al. Haemoglobin, haematocrit and red blood cell indices in elite cyclists: are the control values for blood testing valid? Int. J. Sports Med. 21: 380–385, 2000.
25. Selby, G. B., and E. R. Eichner. Endurance swimming, intravascular hemolysis, anemia, and iron depletion: new perspective on athlete’s anemia. Am. J. Med. 81: 791–794, 1986.
26. Spodaryk, K. Haematological and iron-related parameters of male endurance and strength trained athletes. Eur. J. Appl. Physiol. Occup. Physiol. 67: 66–70, 1993.
27. Weight, L. M., M. Klein, T. D. Noakes, and P. Jacobs. “Sports anemia”: a real or apparent phenomenon in endurance-trained athletes? Int. J. Sports Med. 13: 344–347, 1992.
28. Wilkerson, J. E., B. Gutin, and S. M. Horvath. Exercise-induced changes in blood, red cell, and plasma volumes in man. Med. Sci. Sports 9: 155–158, 1977.
Keywords:

HEMOGLOBIN; CYCLING; RUNNING; IRON METABOLISM; PERFORMANCE

©2002The American College of Sports Medicine