Br J Sp Med 1991; 25(4)

Intravascular haemolysis in the recreational runner

Ronald W. Deitrick PhD, FACSMDepartment of Health, Physical Education and Recreation, California State Polytechnic University, Pomona,California 91768-4079, USA

Intravascular haemolysis has been found to result fromprolonged endurance competition, rigorous military train-ing and participation in impact sports. Haematologicalresearch involving the recreational runner is sparse.Recreational runners frequently vary their training toavoid monotony and improve endurance capacity. Thisstudy investigated the haematological effects of a typicalday of increased distance training in 15 male recreationalrunners (62.4(3.1) ml kg-1 min-' treadmill Vo2max;44.6(8.4) km per week training (mean(s.d.)). Venous bloodsamples were collected before, immediately after, 1 day, 4days, and 10 days after a 13-km training run (about twicethe subjects' typical running distance) and analysed forchanges in bilirubin, serum potassium, haematocrit,haemoglobin, red blood cell count, haptoglobin, poikilo-cytosis and reticulocytosis. Urine samples were collectedat the same times as the blood samples and analysed forurobilinogen. Significant (P < 0.05) 1-day and 4-daydecreases in mean haemoglobin, red blood cell count, andhaptoglobin values, compared to before training venousblood values and significant (P < 0.05) post-trainingincreases in bilirubin, serum potassium, urobilinogen andpoikilocytosis provided evidence for increased intravascu-lar haemolysis. After 10 days the values for haematocrit,bilirubin, serum potassium, red blood cell count, uro-bilinogen and poikilocytosis were not significantly(P > 0.05) different from pre-training values while haemo-globin remained significantly (P < 0.05) lower, exhibitinga constant but not significant increase over the period from1 to 10 days. The results indicate that mild intravascular'footstrike' haemolysis can occur in the recreational runnerwhen typical training distance is increased. This conditionappears to be transient and benign.

Keywords: Running, training effects, sports haematology,endurance exercise

Sports anaemia is a term which has been used todescribe both pseudodilutional anaemia and the trueanaemias of athletes. Pseudodilutional anaemia is anormally occurring and beneficial adaptation toendurance training which is characterized by anovercompensation, that is expansion, of plasmavolume. The two most common causes of trueanaemia in athletes are iron deficiency and intravas-

Address for correspondence: Ronald W. Deitrick, HPERDepartment - Sportsmedicine Research Clinic, California StatePolytechnic University, 3801 West Temple Avenue, Pomona, CA91768-4079, USA© 1991 Butterworth-Heinemann Ltd0306-3674/91/040183-05

cular ('footstrike') haemolysis' which results inurinary loss of iron. Increased intravascular haemo-lysis has been observed to occur as a result ofrigorous military training2 and from participation inimpact sports3 . It has also been recognized in unfitindividuals suddenly subjected to a strenuous bout ofexercise5 and in highly trained endurance athletesafter marathon6 and ultra-endurance competition7 8.More recently, an intensive training programmeconsisting of vigorous isometric and isotonic exer-cises9 and high amounts of training in well-trainedmiddle- and long-distance runners10 has been investi-gated and shows evidence of increased intravascularhaemolysis. No evidence exists regarding the haem-atological effect of a typical increased daily trainingdistance on the moderately trained, 'recreational',endurance runner.

Despite some newer forms of aerobic exercise suchas aerobic dance and cross-training sports like thetriathlon, running continues to be extremely popular.It is estimated that there are more than 30 millionrunners in the USA alone. The great majority of theseindividuals are not competitive runners. However,they do alter their training so as to avoid monotonyand to improve their cardiorespiratory endurancecapacity. The haemolytic effects of such changes intraining in the recreational runner remain largelyunexplored.The purpose of this study was to examine the effect

of increasing the distance of a daily training run, by atypical amount, on the development of intravascularhaemolysis in moderately trained endurance run-ners. Haematological, morphological and urinalysismeasures were selected to study the effects and timecourse changes during recovery.

Patients and methodsFifteen endurance trained Caucasian menvolunteered to participate in this study. Each subjecthad been running 32-56km per week and possesseda maximal oxygen consumption (VO2max) in the rangeof 55-65 ml kg-1 min-'. All testing procedures werecarefully explained and each subject signed aninformed consent form before participating. A train-ing questionnaire was also completed at this time.Percentage body fat was determined as described byZuti and Golding"1. Table 1 displays the physical andphysiological characteristics of the subjects whileTable 2 presents their training characteristics.

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Table 1. Physical and physiological characteristics of malerecreational runners

Variables Mean(s.d.) Range

Age (years) 27.8(6.3) 19-40Height (cm) 172.5(23.8) 165-190Weight (kg) 70.6(7.3) 60.5-85Body fat(%) 12.1(3.7) 7.4-20.3Vo2max (mlkg- min-) 62.4(3.1) 55.2-65.6

n = 15

Table 2. Training characteristics and environmental conditions for13-km training run

Variables Mean (s.d.) Range

Weekly distance (km) 44.6(8.4) 32-56Distance per run (km) 8.9(1.6) 6.4-11.2Frequency per week 4.7(0.9) 3-6Time for training run (min: s) 55:19(3:55) 50:22-62:30Ambient temperature ('C) 22.3(1.1)Relative humidity (%) 54(4.3)

n = 15

To determine VO2max, each subject underwent acontinuous, progressive, multistage treadmill test.The protocol consisted of a brief warm-up followedby an initial exercise intensity of 188m min' at a 4%grade (this represents a treadmill elevation of fourvertical units for every 100 horizontal units) with a2.5% increase in grade every 2min thereafter, whilekeeping speed constant. Verbal encouragement wasgiven throughout the test, especially at the highestlevels of exercise intensity. Oxygen consumption wasdetermined at 30-s intervals using a BeckmanMetabolic Cart (MMCI, Beckman Instruments, Brea,California, USA). Criteria for V02 max included aplateau in oxygen consumption (less than2rmlkg-'min-1 increase with a further increase inworkload), a respiratory exchange ratio greater than1.1, and approximation (within ten beats per minute)of age predicted maximum heart rate. With a majorityof the criteria satisfied, the highest rate of oxygenconsumption achieved was recorded as VO2max.Heart rate was monitored continuously by anelectrocardiogram using a CM5 lead placement(negative electrode on manubrium, positive electrodeon 5th intercostal space, left anterior axillary line).

After treadmill testing, three separate days werescheduled for the 13-km run with the time of day(mid-morning) held constant. The course was flat andevery subject ran it once within a week. The coursesurface comprised a mixture of dirt and gravel (thesoft shoulder of a road) with occasional stretches ofblacktop. Seven of the 15 subjects ran on the firstscheduled day, four ran on the second day and fourran on the last day. The subjects were instructed notto run longer than their average daily trainingdistance for at least 4 days before the 13-km run whilemaintaining average daily training intensity, and alsoto resume typical training distances after the 1-dayblood draw but not to do any longer or more intense

runs than they would normally do until after the finalblood draw. The intention was to observe theselected variables during the normal course oftraining in a group of recreational runners with aminimum of experimental interference.On the day of the run, subjects were instructed to

run the 13km as though it was a hard training run.They were reminded not to compete with each otherbut rather to run at a training pace that was typical forthem, for this distance. Subjects ran on the same dayonly for ease of post-run data collection. Each subjectagreed at the end of the 13km that his effort wassimilar to a typical hard training run as indicated onthe training questionnaire. The environmental condi-tions and times for the training run are shown in Table2.With the subject seated, fasting venous blood

samples (12 ml total per draw) were collected by anexperienced certified phlebotomist for analyses be-fore the increased distance training run and atselected times after the run (within 1 h, 1 day, 4 daysand 10 days). The pre-training run values wereconsidered to be representative of typical trainingstatus. Extreme care was taken during the venepunc-ture to avoid the possibility of any haemolysis fromthe blood draw itself. All samples were transportedon ice to a nationally accredited (joint Commission onAccreditation for Hospitals) clinical laboratory. Usinganti-coagulated ethylene diamine tetra-acetic acid(EDTA) blood, the haematological assays wereperformed within 4 h after collection by a registeredAmerican Society of Clinical Pathologists (ASCP)medical technologist on a J.T. Baker Model 500Ahaematology analyser (Serono-Baker Diagnostics,Allentown, Pennsylvania, USA) which had beencalibrated immediately before assessment.Serum potassium, total lactate dehydrogenase

(LDH), and bilirubin concentrations were analysedon a Technicon SMA/20 automated analyser (Tech-nicon Instruments, Tarrytown, New York, USA). Thepotassium method was a direct potentiometricprocedure for the quantitative measurement ofpotassium in buffered serum12. The potassiumion-selective electrode responds to potassium ionsaccording to the Nernst equation. Total LDH determi-nation was based on methods and modificationspreviously described13. The total bilirubin methodwas a quantitative calorimetric procedure'4. Assaysfor haptoglobin were determined using M-Partigenhaptoglobin kits containing radial immunodiffusionplates obtained from Calbiochem-Behring Corpor-ation (Behring Diagnostics, Somerville, New Jersey,USA). All procedures and calculations were con-ducted in accordance with the instructions accom-panying the kits and met all the criteria specifiedtherein.

All urines were collected in standard urinalysisspecimen containers and analysed immediately aftercollection. Urobilinogen was determined on the urinespecimens using Ames multistix reagent strips(Miles, Diagnostics Division, Elkhart, Indiana, USA)and following the accompanying instructions. Usinga Wright's stained blood smear of anticoagulatedblood (EDTA as the anticoagulant), poikilocytosiswas observed and rated 0, +1, +2, +3 or +4

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following the standard procedure employed by themedical laboratory responsible for the morphologicalevaluation. Reticulocytosis was measured microsco-pically using a drop of new methylene blue anti-coagulated blood mixture. Reticulocytes were enum-erated in red blood cell counts of a thousand andexpressed as a percentage. All blood and urineanalyses were performed by registered (ASCP)medical technologists who were unaware of thepurpose of the study.A single-group repeated-measures research design

was used for this study with statistical significancedetermined by analysis of variance. The repeatedmeasures research design allows for the highestdegree of comparability among subjects (since sub-jects serve as their own controls) and is the dictateddesign when the study involves measuring the samegroup of subjects over time to assess effects whichdevelop with the passage of time'5. Additionally, therepeated measures design provides a means ofincreasing the number of subjects in a study. Onelimitation of such a study design is the possibility ofcarry-over effects. This was perhaps a limitation inthis study since the subjects were permitted toresume normal training after the 1-day blood draw.However, the study was designed to provide for anassessment of the haematological effects of a typicalincrease in training distance in a realistic trainingsetting. This necessitated the resumption of trainingfollowing the 13-km run. Using selected orthogonalcontrasts, post hoc analyses were conducted to probefor significant differences when indicated. Resultswere judged significant where P < 0.05.

ResultsThe endurance runners in this study averaged44.6 km of running per week while training, onaverage, 4.7 times per week and 8.9km per run (Table2). The mean maximal oxygen consumption value of62.4 ml kg min' for this group is greater than thetypical VO2max value of 39.1 ml kg-' min' reported for

individuals ofthis age and sex"6; lowerthan the value of70-85 ml kg-' min' reported for elite male endurancerunners'7; and similar to the 60.6 ml kg-l min'reported for other male recreational runners'8. Inaddition, these runners were leaner than the averageman for their age group, 12.1% versus 20.1% body fat'6and not as lean as high calibre endurance athletes:12.1% versus 5-8% body fat'7.Only two of the runners had run in a race (both

10km) during the 6 months before the study, andnone had ever run a half or full marathon. The 13-kmtraining run represented the average distance of whatthe runners in this study currently used as anincreased, once a week, training distance, as statedon the training questionnaire. The range of distancesused for this purpose varied from 9.6km to 16kmwith about half of the study group reporting 13km.Evidence for the increased effort required to completethis increased training distance can be seen in thesignificantly (P < 0.05) elevated LDH levels asmeasured within 1 h after the training run andcompared to the pre-training run values (Table 3).The mean haematological values for haematocrit,

haemoglobin, red blood cell count, haptoglobin andmean cell volume for each of the measurement timeperiods assessed are shown in Table 3. The haemato-crit and red blood cell values increased significantly1 h after the increased distance training run whencompared to their respective pre-training run values,after which time both decreased significantly; that is,1-day values were significantly lower than 1-hpost-training values for these two variables. Redblood cell values were significantly lower thanpre-training run values when measured 1 day and 4days afterwards. The haemoglobin concentrationmeasured 1 day after the increased distance trainingrun was significantly decreased from the pre-trainingrun values and remained so when measured 4 daysand 10 days after the run.Haptoglobin was significantly lower 1 day and 4

days after the increased distance training run butreturned to pre-training run values by the tenth day.

Table 3. Blood and urine responses to increased distance training run*

Variables Pre-training Post-training runrun

lh 1 day 4 days 10 days

Clinical chemistryLactate dehydrogenase (U 1-1) 190.7(32.1) 236.8(43.4)t 207(30.8) 192.2(37.1) 195.4(32.9)Bilirubin (mgdI-1) 0.6(0.1) 0.8(0.2)t 0.7(0.2) 0.6(0.2) 0.6(0.1)Serum K+ (meq 1-1) 4.5(0.4) 4.8(0.6)t 4.6(0.6) 4.3(0.4) 4.4(0.4)

HaematologyHaematocrit (%) 44.5(1.7) 45.9(2.6)t 43.6(1.4)t 44.2(1.7) 44.5(1.6)Haemoglobin (gdl-1) 15.6(0.5) 15.8(0.7) 15.1(0.3)tt 15.0(0.4)t 15.2(0.5)tRed blood cell (106 mm-3) 5.02(0.26) 5.17(0.31)t 4.86(0.19)tt 4.88(0.34)t 4.95(0.29)Haptoglobin (gl100mV1) 91.9(69.1) 80.4(75.1) 66(65.8)t 59.5(52.9)t 81.8(63)Mean cell volume ([Lm3) 89(3.9) 89.3(3.5) 89.6(2.8) 90.6(3.9) 89.8(3.2)

UrinalysisUrobilinogen (Ehrlich units dV-1) 0.1(0) 0.8(0.4)t 0.4(0.4)tt 0.1(0)§ 0.1 (0.2)§

MorphologicalPoikilocytosis (0, +1, +2, +3 or +4) 0 0.33(0.48)t 0.4(0.5)t 0.4(0.5)t 0.1(0.2)Reticulocytosis (%) 0.55(0.27) 0.56(0.21) 0.61(0.28) 0.71(0.23) 0.64(0.15)

* Values are means(s.d.); n = 15; t significantly (P < 0.05) different from pre-training run; t significantly (P < 0.05) different from 1 h afterthe training run; § significantly (P < 0.05) different from 1 day after the training run

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Serum potassium and bilirubin were initially signifi-cantly elevated, as measured within 1 h after thetraining run, but were not significantly different frompre-training run values when measured thereafter(Table 3). LDH, haptoglobin and serum potassiumwere the only variables outside the normal rangeduring any of the measurement times, and all of thevariables selected for the study were in the normalrange at the start of the study and at the end (10 daysafter the training run). They were only outside therange after the 13-km run.

Urobilinogen was significantly elevated 1 h and 1day after the increased distance training run andreturned to within the normal range thereafter asmeasured 4 days and 10 days after the training run(Table 3). Morphological changes following theincreased distance training run are also shown inTable 3. Poikilocytosis was significantly elevated 1 h, 1day and 4 days following the training run ascompared with pre-training values, while there wasno significant change in reticulocytosis at any of themeasurement times selected for this study.

DiscussionThis study was designed to examine the effects of atypical change in endurance training, an increaseddistance run, on the haematological state of thenon-competitive distance runner. Based on theinformation obtained (physiological, body composi-tion measures, training and current competitionstatus) and a comparison of this with high calibredistance runners, the subjects in this study can bedescribed as a typical group of recreational runners.The great majority of people who run as a means ofimproving cardiorespiratory fitness and maintainingbody composition, fall into this non-competitiverecreational category; and yet, little if any haematolo-gical research has been carried out using them asstudy subjects. One of the reasons they are ofinterest, aside from their numbers, is that out of thisgroup will come a number of dedicated andenthusiastic distance runners who will train harderand longer, eventually making the transition to ahighly competitive state. An understanding of theacute haematological changes in the recreationalrunner may provide an insight into how the knownhaematological adaptations, both positive and nega-tive, occur in the highly competitive distance runner.

It is known from research regarding the competi-tive distance runner, that regular prolonged exercisebrings about diverse haematological responses andadaptations. Among the haematological responses inthe high calibre distance runner are gastrointestinalbleeding19 and an increased intravascular haem-olysis8'10 20. Adaptations include beneficial effectssuch as dilutional pseudoanaemia21 and an increasedred cell mass22 as well as a possible iron-deficientanaemic state23'24 which is detrimental to perform-ance. The purpose of this study was to investigatewhether or not a typical increase in daily trainingdistance would increase intravascular haemolysis inthe non-competitive, recreational distance runner.

Eichner21 has suggested a diagnostic triad for

footstrike haemolysis that includes subnormal hapto-globin concentration, mild reticulocytosis, and mildmacrocytosis. Other researchers have noted increasesin bilirubin, serum potassium and LDH, and de-creases in red blood cell volume and haematocrit, tobe indicators of increased intravascular haem-olysis20 25. Most researchers have used a transientdecreased concentration of haemoglobin to identify'sports anaemia'26, the primary cause of which hasbeen attributed to intravascular haemolysis27. Theathlete's state of hydration is an important consider-ation when deciding which of the criteria to use.Body weight has been shown to be a valid andreliable indicator of hydration state28. In the currentstudy, mean body weight as measured 1 day after therun and compared to the pre-training run mean(s.d.)(70.3(6.8) versus 70.6(7.3) kg) was not significantlylower (P > 0.01).

It can be concluded from the results of this studythat intravascular haemolysis also occurs in therecreational runner. Evidence for this includedsignificant 1-day decreases in haptoglobin, haemo-globin, red blood cell and haematocrit and theimmediate post-training run increases in bilirubin,serum potassium and urobilinogen. Morphologicalevidence included significant increases in poikilocy-tosis as measured 1 h, 1 day and 4 days after theincreased distance training run, and increases inreticulocytosis and mean cell volume 4 days after-wards which were not significant. With the exceptionof haemoglobin, all of the observed significantchanges following the increased distance training runreturned to pre-training run levels by the tenth dayafter the run.The increased intravascular haemolysis that occur-

red in this study with these recreational runners canbe described as transitory and mild; transitorybecause of the non-significant variable differencesobserved on the tenth day after the training run ascompared with pre-training values. Other studiesusing highly trained subjects have reported decreasesin haemoglobin of up to 2.6gdl-1 (reference 8) andhaptoglobin to be exhausted following marathonrunninge, while this study noted a mean drop of30% in haptoglobin and only a modest (0.6gdl-1)decrease in haemoglobin. However, five subjects inthe study exhibited a mean decrease of haemoglobingreater than 1.0gdl-1, with the greatest decrease inhaemoglobin being 1.6gdl-'. The findings of thisstudy with respect to haptoglobin and haemoglobinare similar to those reported recently for aerobicdance4.

In contrast to other research investigations ofsports anaemia, this study suggests that intravascularhaemolysis may be a relative phenomenon thatoccurs even in the recreational runner when adjust-ments to typical training distances are made. Theresults indicate that this transient condition is bestassessed by immediate post-exercise bilirubin, serumpotassium and urobilinogen determinations; and by1-day post-exercise measurements of haptoglobin,haemoglobin and red blood cells. Since haemoglobincontinued to be significantly decreased 4 days and 10days after the increased distance training run, itmight be advisable to moderate training for the next

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several days to ensure complete haematologicalrecovery.The increased intravascular haemolysis in the

recreational runner may be a contributing stimulusfor the beneficial cardiorespiratory endurance adapt-ation of erythrocythaemia or might even be importantin bringing about an optimal haematological state forperformance, which seems to be a borderline anaemicstated. Further haematological research is neededregarding the repeated effects of such changes intraining, including intensity as well as distance, overa longer period of training, and their relationship toperformance.

AcknowledgementsThe author wishes to thank Mary Lou Rodriguez forher preparation of the paper.

References1 Eichner ER Other medical considerations in prolonged

exercise. In: Lamb DR, Murray R, eds. Perspectives in ExerciseScience and Sports Medicine, vol 1: Prolonged Exercise. Indianapo-lis, Indiana, USA: Benchmark Press, 1988: 420.

2 Radomski MW, Sabiston BH, Isoard P. Development of'sports anemia' in physically fit men after daily sustainedsubmaximal exercise. Aviat Space Environ Med 1980; 51: 41-5.

3 Streeton JA. Traumatic haemoglobinuria caused by karateexercises. Lancet 1%7; ii: 191-2.

4 Schwellnus NP, Penfold GK, Cilliers JF, Kuyl JM, van derHeever DP. Intravascular hemolysis in aerobic dancing: therole of floor surface and type of routine. Phys Sportsmed 1989;17: 55-67.

5 Schmidt W, Maasen N, Trost F, Bowing D. Training inducedeffects on blood volume, erythrocyte turnover and hemoglo-bin oxygen binding properties. Eur I Appl Physiol 1988; 57:490-8.

6 Casoni I, Borsetto C, Cavicchi A, Martinelli S, Conconi F.Reduced hemoglobin concentration and red cell hemoglobini-zation in Italian marathon and ultramarathon runners. Int jSports Med 1985; 6: 176-9.

7 O'Toole ML, Hiller WDB, Roalstad MS, Douglas PS.Hemolysis during triathlon races: its relation to race distance.Med Sci Sports Exerc 1988; 20: 272-5.

8 Dressendorfer, RH, Wade CW, Amsterdam EA. Develop-ment of pseudoanemia in marathon runners during a 20-dayroad race. JAMA 1981; 246: 1215-18.

9 Magazanik A, Weinstein Y, Din RA, Derin M, SchwartzmanS, Allabouf D. Iron deficiency caused by 7 weeks of intensivephysical exercise. Eur I Appl Physiol 1988; 57: 198-202.

10 Dufaux B, Hoederath A, Streitberger I, Hollmann W,Assmann G. Serum ferritin, transferrin, haptoglobin, and

iron in middle- and long-distance runners, elite rowers, andprofessional racing cyclists. Int I Sports Med 1981; 2: 43-6.

11 Zuti WB, Golding LA. Equations for estimating percent fatand body density of active adult males. Med Sci Sports 1973; 5:262-70.

12 Rao J, Pelavin MH, Morgenstern S. SMAC high-speedcontinuous-flow, ion-selective electrodes for sodium andpotassium: theory and design. In: Advances in automatedanalysis, technicon international congress 1972, Vol. 1: ClinicalChemistry Methods, New York, USA: mediad, 1973: 33-6.

13 Morgenstern S, Flor R, Kessler G, Klein B. Automateddetermination of NAD coupled enzymes, determination oflactic dehydrogenase. Anal Biochem 1965; 13: 149-61.

14 Gambino SR, Schreiber H. The measurement and fractiona-tion of bilirubin on the autoanalyzer by the method ofJendrassik and Graf. In: Automation in analytical chemistry,technicon symposia, New York, USA: mediad, 1965: 42-6.

15 Dayton CM. The Design of Educational Experiments. New York,USA: McGraw-Hill, 1970: 245.

16 Pollock ML, Wilmore JH, Fox SM. Health and fitness throughphysical activity. New York, USA: John Wiley and Sons, 1978:266-7.

17 Costill DL, Winrow E. Maximal oxygen intake amongmarathon runners. Arch Phys Med Rehab 1970; 51: 317-20.

18 Ramsbottom R, Williams C, Boobis L, Freeman W. Aerobicfitness and running performance of male and femalerecreational runners. I Sport Sci 1989; 7: 9-20.

19 Fisher RL, McMahon LF, Ryan MJ, Larson D, Brand, M.Gastrointestinal bleeding in competitive runners. Dig Dis Sci1986; 31: 1226-8.

20 Lindemann R, Ekanger R, Opstad PK, Nummestad M,Ljosland R Hematological changes in normal men duringprolonged severe exercise. Am Corr Ther 1 1978; 32: 107-11.

21 Eichner ER The anemias of athletes. Phys Sportsmed 1986; 14:122-30.

22 Brotherhood J, Brozovic B, Pugh LGC. Haematological statusof middle- and long-distance runners. Clin Sci Mol Med 1975;48: 139-45.

23 Hunding A, Jordal R, Paulev PE. Runner's anaemia and irondeficiency. Acta Med Scand 1981; 209: 315-18.

24 Ehn L, Carlmark B, Hoglund S. Iron status in athletesinvolved in intense physical activity. Med Sci Sports Exerc 1980;12: 61-4.

25 Wolf PL, Lott JA, Nitti GJ, Bookstein R Changes in serumenzymes, lactate, and haptoglobin following acute physicalstress in international-class athletes. Clin Biochem 1987; 20:73-7.

26 Pate RR Sports anemia: a review of the current researchliterature. Phys Sportsmed 1983; 11: 115-31.

27 Yoshimura H. Anemia during physical training (sportsanemia). Nutr Rev 1970; 28: 251-3.

28 Young AJ, Sawka MN, Dennis RC, Pandolf KB, Valeri CRBlood volume variability due to anthropometric factors andaerobic fitness. Med Sci Sports Exerc 1990; 22: S135.

29 Eichner ER Runner's macrocytosis: a due to footstrikehemolysis. Runner's anemia as a benefit versus runner'shemolysis as a detriment. Am J Med 1985; 78: 321-5.

30 Crowell JW, Smith EE. Determinant of the optimal hemato-crit I Appl Physiol 1967; 22: 501-4.

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