Br. J. Sp. Med; Vol 23

Review

Blood doping - a literature review*

Mark Jones' MB, BS, Dip Sports Med and Dan S Tunstall Pedoe2 DPhil, FRCP

There is increasing evidence that the technique of reinfus-ing an athlete's stored blood prior to competition to im-prove performance has been used on many occasions.Although early experimental results were controversial andthe precise mechanism by which the technique improvesperformance is still debated, there is now strong evidencethat if the blood doping produces a sufficient rise in totalred cell mass there are significant improvements inphysiological variables such as maximum oxygen uptake,lactate buffering and thermoregulation. These physiologi-cal changes are matched by improvements in enduranceperformance. These may persist in diminishing degree forseveral weeks, but have to be weighed against the detrain-ing effect produced by the repeated venesection required toobtain an adequate amount of stored blood for autologousreinfusion.

Experimental evidence suggests that the transient in-crease in blood volume and cardiac output following rein-fusion is too short lived to be of any real importance and themajor effect is related to the increase in total red blood cellmass and haemoglobin enabling an increased transport ofoxygen and therefore a potentially greater reserve of bloodwhich can be diverted to non-exercising tissues to improvethermoregulation. The increased red cell mass also im-proves lactate buffering. Although these benefits have beenshown in several studies the increases in performance andmeasured physiological parameters do not bear a directrelationship to the changes in haematological variables.Blood doping is of considerable importance, not only as

an abuse of fair competition, but also because of the light itthrows on the physiological limits to endurance perform-ance. It has reawakened controversy as to whether oxygentransport is the limiting factor in endurance.

DefinitionsBlood doping, blood boosting, blood packing or inducederythrocythaemia are terms used to describe the infusion ofred blood cells to increase aerobic power.Autologous blood doping refers to the infusion of the sub-

ject's own stored blood.

'Dr MarkJones, 64 Seaforth Avenue, Oatley, Sydney, Australia 22232Dr Dan S. Tunstall Pedoe, Medical Director, The London SportsMedicine Institute, c/o Medical College of St Bartholomew'sHospital, Charterhouse Square, London EC1M 6BQ

*This literature review is a shortened and edited version of a thesissubmitted by Dr Mark Jones as part of the London Hospital SportsMedicine Diploma Course June 1988.

©) 1989 Butterworth & Co (Publishers) Ltd

0306-3674/89/020084-05 $03.00

84 Br. J. Sp. Med., Vol. 23, No. 2

Heterologous blood doping involves the infusion of bloodfrom one or more cross-matched donors.

Techniques of blood doping

Heterologous blood doping

Use of a matched blood donor has the advantage thatthe athlete does not have to suffer the detraining ef-fects of venesection. The blood can be used im-mediately and, if so, has not suffered any deleteriouseffects from storage. The disadvantages are the poten-tial transfer of infection, such as hepatitis and AIDS,and possibilities of transfusion reactions. Heterolog-ous blood transfusion or packing is also easier to detectwith an appropriate blood sample.

Autologous blood dopingAutologous blood doping involves removing twounits of the athlete's blood, storing the blood and thenreinfusing it about seven days prior to the athletic con-test. Venesection needs to be performed at least threeweeks before reinfusion to allow the subject's haemo-globin to recover to normal levels1. An interval of eightto twelve weeks is preferable in order to allow theathlete not only to regain his haemoglobin, but to getback to his previous level of fitness and overcome thedetraining effect of blood donation2.The utility of autologous blood doping depends

very much on how the blood is stored.

Conventional storageIn the conventional blood bank method, whole bloodis citrated and refrigerated at 40C. Despite the additionof preservatives and anticoagulants, the blood de-teriorates steadily, the red cells becoming progres-sively less flexible and more fragile3'4. There is anincrease in blood viscosity resulting from this' andincreased brittleness of the red cells means that thesecells can fragment on reinfusion1'5. Six to seven per-cent of the stored red cells are lost each week andbecause of this steady deterioration blood is not trans-fused after three weeks of conventional storage in theUnited States of America and after four weeks in Scan-dinavia. By that time between 30 and 40 per cent of thered blood cells may have been lost or be of no practicalbenefit when reinfused6.

Conventional blood storage therefore is of minimal,if any, practical use for autologous blood doping, but

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could be used as a short term measure for heterolog-ous blood transfusion. For autologous blood doping,the athlete is unlikely to have recovered fully fromblood donation by the time the blood is transfusedback and so although there may be some improvementabove previous peak performance, the full potentialadvantage would not be gained.

High glycerol freezingAn elaborate technique can be used for almost indefi-nite storage of red cells"4. This technique is usedroutinely for rare blood types and is being increasinglyused for autologous blood transfusion where patientsare facing a major operation and only wish to receivetheir own blood. The blood is centrifuged and glyceroladded to the high concentration of red cells which arethen frozen at -80°C in liquid nitrogen. For reinfu-sion, the cells are carefully thawed and undergo aseries ofwashes of increasing osmolality to remove theglycerol. They are then resuspended in normal salineand reinfused in a suspension with haematocrit ofapproximately 50 per cent.The ageing of the red blood cells is suspended by

freezing and there is a total loss of only 15 per cent ofthe red cells during the total handling process" 6. Bloodcan be stored for up to ten years using this techniqueand the technique maximises the recovery of red bloodcells and ensures that an adequate interval can be ob-tained between venesection and reinfusion of theblood for blood doping.

Hypotheses and experimental basis ofblood dopingBlood doping could be ergogenic through its effect onoxygen carriage by producing a polycythaemia andblood volume and cardiac output.

Oxygen carriageSupporters of blood doping claim that it increases oxy-gen carriage by the blood. As each gram of haemo-globin if fully saturated carries 1.34 ml of oxygen, anincrease of, say, 2 g of haemoglobin per 100 ml bloodincreases potential oxygen carriage per litre of bloodby, say, 25 ml. Assuming a mixed venous saturation offifty per cent, half of this would be available at theworking muscle and at an exercise cardiac output of,say, 24 litres per minute 300 ml of extra oxygen couldbe delivered to the tissues.Improved performance would only occur if exercise

cardiac output was maintained and was unaffected bythe increased blood viscosity implicit in raising thehaematocrit or if the exercising muscles could use theadditional oxygen and therefore work harder. The ex-perimental evidence is described below.

Blood volume, stroke volume and cardiac output

Endurance exerciseEndurance athletes when compared with normal con-trols usually have an increased blood volume, with anabove normal total red cell mass (up to 20 per centincrease), and plasma volume, the latter often in-

creased to a greater degree" 2'7-'0. This often gives riseto a reduction in haemoglobin concentration and socalled athletes anaemia or pseudoanaemia, which hasbeen well documented. (See Review, pp 81.)The increased blood volume of endurance athletes

gives the heart a greater preload and thus improvedstroke volume and maximum cardiac output. This, to-gether with the improved vascularization of the mus-cle which results in greater oxygen extraction from theblood (lower mixed venous blood oxygen saturation),helps the athlete obtain very high levels of oxygen up-take and utilization for sustained periods of endurancework. The increased plasma volume also allows agreater blood flow to the skin to help dissipate heatand gives a greater latitude for dehydration. Since theendurance athlete often has a low haematocrit with abelow normal blood viscosity, dehydration is poten-tially better tolerated since both hypovolaemia and arise in blood viscosity to above normal levels would re-quire a much greater fluid loss.

Blood transfusionBlood transfusion does produce a transient increase inblood volume, stroke volume and cardiac output butwork by Guyton and Richardson1'1,2 shows that thiseffect only lasts a few minutes in experimental animalssince the increased capillary pressure causes plasmatransudation and loss of blood plasma which buffersany attempt to increase blood volume artificially'3'4.Studies in man show most plasma shift has occurredwithin one hour of transfusion and whole blood trans-fusion has the same effect as giving packed cells in thenormal subject, a normovolaemic polycythaemial15' 6.There is no measurable increase in blood volume 24hours later617'18, whether measured indirectly orusing a labelled albumin method to confirm bloodvolume'8"9.

In a series of studies on five healthy young men,Kenstrup and Ekblom showed that V02 max appearedto be directly related to the total red cell mass ratherthan the blood volume or the haemoglobin concentra-tion3. Blood withdrawal caused a fall in V02 max whichwas not increased by volume expansion. Volume ex-pansion alone causing a drop in haemoglobin had noeffect on VO2 max whereas a reinfusion of red bloodcells causing an elevated haemoglobin concentrationand total red blood cell mass increased the V02 max-These findings reinforce the view that the endurancerunner with a raised total red cell mass but a low nor-mal haemoglobin (i.e. runners pseudoanaemia) is notat any physiological disadvantage compared with arunner with the same total red cell mass but a smallerplasma volume.The other postulated benefits of blood doping with

respect to endurance exercise performance are relatedto lactate buffering and thermoregulation.

Lactic acid bufferingThe accumulation of lactic acid in exercising musclelimits contractile performance by direct inhibition ofenzyme systems within the muscle20. Reduction in lac-tate production or increased buffering of the lactate tomaintain the muscle pH within more normal limitswould act as a considerable ergogenic aid'8. One of themain acid/base buffering systems in the body is blood,

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and red blood cells are responsible for 70 per cent ofthe buffering capacity of blood21. An increased totalred cell mass therefore increases the buffering capacityfor lactic acid22 and therefore allows a greater degree ofanaerobic exercise before the muscles become inhi-bited by the acidity6'18'21. In old fashioned terms, theathlete can achieve a greater 'oxygen debt'. This effectis in addition to the greater aerobic power followingblood doping17'19'23.ThermoregulationThe transport functions of the blood during exerciseare not only that of supplying active muscle with fueland oxygen and carrying away the metabolic productsof muscular activity, but also to transport heat awayfrom the exercising muscle and to enable it to be dissi-pated without the core temperature of the athlete ris-ing to dangerous levels. In many forms of enduranceexercise, particularly in hot conditions, a significantpart of the cardiac output is involved in heat dissipa-tion with blood being shunted through the superficiallayers of the skin to dissipate this heat. This part of thecardiac output is therefore not available for the trans-port of oxygen to the exercising muscle; thus, perfor-mance is limited. If, because of a raised haematocritfrom blood doping, a smaller proportion of the totalcardiac output can supply the same amount of oxygento exercising muscle, this releases a larger componentof the output for this secondary role of heat dissipationwhich can therefore be more efficient and will allow a

higher work rate in unfavourable environmental con-ditions. Studies by Sawka et al. on exercise in a hotenvironment suggest that infusion of 900 ml of auto-logous freeze-preserved blood confers considerableadvantages in terms of thermoregulation during en-durance exercise

Experimental evidence for beneficial effectsof blood dopingA large number of studies have been performed onblood doping and the results of many of these areshown in Table 1. The evidence from those studies inwhich a significant rise in haemoglobin and haemato-crit was achieved, is that the major effects of blooddoping are through the effect on oxygen carriage. Theeffect on cardiac output and blood volume is transientand the increased endurance capacity seems therefore tobe based on an increased red cell mass and haematocrit.The first study by Pace et al. in 194724 showed that

transfusion of 2000 ml of matched blood into reci-pients caused a considerable increase in haemoglobinand endurance time. Subsequent studies using refrig-erated blood in smaller amounts have been much lessspectacular and in some cases have shown changeswhich have been barely significant. The overwhelm-ing impression from the studies shown in Table 1is that if sufficient red cells are transfused a defi-nite improvement can be obtained in enduranceperformance.

Table 1. Summary of experimental studies of blood doping6'8

Volumeinfusedofwhole Time ofblood or reinfusion

Number equivalent postof Storage whole blood phlebotomy % increase vs control

Authors Date subjects technique (ml) (weeks) Hct/Hb VO2max Endurance

Pace etal. 1947 fresh 2000 26(a) NR 34.7(a)Gullbringetal. 1960 refrig 610 1 0.7 NR 3Robinson etal. 1966 refrig 1000 2 4.8 1.4 NREkblom etal. 1972 7 refrig 800 4 2.1 5.5(b) 15.6(b)

7 refrig 1200 4 1.3 1.6(b) 25.1 (b)Von Rostetal. 1975 refrig 900 3 2.7 9(b) 37(b)Bell et al. 1976 15 refrig 500 3 1 5.6(b) 7.5Ekblom et al. 1976 5 refrig 800 5 4.5(b) 8.0(a) NRVideman and 1977 10 refrig 4-600 2-3 2.6 NR 3.8RytomaqFrye and Ruhling 1977 16 refrig 500 2.5 NR 0 NRRobertson eta/. 1978 5 frozen 1800 16 NR 12.8(a) 15.8(a)Williamsetal. 1978 16 frozen 460 3 3.3 NR 4.1Cottrell 1979 frozen 405 9 NR 2 NRRobertson et al. 1979 7 refrig 800 NR 15.8(a) 30.5(a) 13.1 (a)Pate et al. 1979 7 refrig 450 3 0 0 NRBuicketal. 1980 11 frozen 900 7 11(a) 5(a) 35(a)Sptriet et al. 1980 4 frozen 800 11 7.9(a) 3.9(a) NRWilliams et al. 1981 12 frozen 920 7 7(a) NR 2.5(a)Goforth et al. 1982 6 refrig 760 4 4.6 11 improvedThomson etal. 1982 4 frozen 1000 12 3.8(b) inc.(a) NRKonstrup and 1983 5 refrig 900 5 2(a) 7(a) 24(a)EkblomRobertson etal. 1984 9 frozen 900 16 18(a) 10(a) 22.8(a)Berglund et al. 1986 6 refrig 1350 4 7.9(a) NR improvedSawkaetal. 1987 6 frozen 900 20 inc. 11(a) NRBrien etal. 1987 6 frozen 900 11 5(a) NR improved(a)

Key: (a) Statistically significant, (b) No statistical analysis reported, NR Not reported, inc. increased

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The improvement in performance is often much lessthan would be predicted from the increased haemo-globin and there is considerable doubt as to the exactmechanism by which the increased endurance capac-ity is achieved.

Early studies used small numbers of volunteerswithout any control subjects and without a doubleblind crossover of the procedures used. More recentstudies such as those of Buick et al.18, Williams et al.2 ,Robertson et al.13' and Brien and Simon9 had muchbetter experimental design, used the high glycerolfreezing technique and all show a significant improve-ment in endurance performance with blood doping.However, the individual variations in improvementremain unexplained even when adequate time (aweek) between the reinfusion and the testing is al-lowed. Reinfused blood takes a finite time to overcomethe effects of storage. In particular, the concentrationof certain enzymes such as 2,3-DPG falls in conven-tionally stored blood and takes 24 hours or more toachieve normal levels. However, this effect is said tobe less marked in glycerol frozen blood.The discrepancies between the rise in haematocrit,

the increase in maximum oxygen uptake and improve-ment in aerobic performances which show an unpre-dictable relationship to each other do raise questionson the exact nature of the ergogenic effects of blooddoping as well as questioning what limits maximalaerobic performance.The centralist theory is that the oxygen transport by

the cardiovascular systems and lungs and its carriagein the blood is the limiting factor is favoured by theproven benefits of blood doping. The lack of a predict-able response to improvements in haematocrit andtotal red cell mass suggest that there may be limita-tions at the muscle level which are also of considerableimportance.

Adverse effects of blood dopingThe demonstrated benefits of blood doping might givethe impression that it is a totally safe procedure. Apartfrom the theoretical risks of transfer of infectious diseasesuch as AIDS and hepatitis, if heterologous transfu-sion is used, any intravenous infusion carries riskssuch as venous thrombosis, phlebitis and septicaemia,particularly if the transfusion is given in less thanadequately sterile circumstances. The raisedhaematocrit, increased viscosity and hypercoagul-ability of blood following transfusion may well becompounded by an athlete spending many hours rela-tively immobile, travelling to the sporting venue andrunning a high risk of venous thrombosis, even pul-monary embolism.

For autologous blood doping, venesection of 500 mlof blood on one or more occasions has a marked de-training effect, and will limit the amount and quality ofthe training in the run up to competition.A possibly anecdotal disadvantage is that the re-

moved blood may contain damning evidence of abanned substance such as an anabolic steroid, taken intraining but stopped well before competition, but thenreintroduced in the stored blood and giving a positivein the urine, when tested at competition for bannedsubstances.

The detection of blood dopingBlood doping is banned by IOC doping regulations. Itis generally recognised as a form of cheating. How-ever, there is no easy way of detecting blood doping.It is easy therefore both for an athlete to cheat and getaway without being detected, and also for an athlete tobe accused unfairly of blood doping and not be able tovindicate himself. It is the only doping ban that cannotpresently be supported by testing.The International Olympic Committee has funded

Berglund to try to find a method of detecting blooddoping but so far methods of detection have been dis-appointing. Infusion of conventionally refrigeratedblood does produce a rapid increase in serum iron andbilirubin and a drop in serum erythropoietin. Unfor-tunately, serum erythropoietin is suppressed by phys-ical exercise so low levels after competition are notdiagnostic. Berglund has produced an algorithm to de-tect blood doping based on his studies5' ', but this haslimited sensitivity. So far his studies have used con-ventionally refrigerated, rather than glycerol-deep-frozen, blood in athletes living and training at sealevel.Heterologous transfusion could be detected by

showing red cells carrying foreign non-ABO bloodgroups, since a complete match of all groups would bestatistically a remote possibility (unless the runner hada twin).

It has been suggested that one of the best methodsof detecting blood transfusion would be by showing anon-uniform distribution in the red cell size (which isinfluenced by the age of the red blood cells), but thistechnique is not yet practical26.

All techniques of detection require at least one bloodsample, and most require several for definite evidenceof blood doping to be proven. At the moment, athletesare subjected to urine, but not blood sampling and thedetection of blood doping therefore remains a majorproblem for the athletic authorities.

Since trace substances in infused blood are detect-able, possibly the only practical way of detecting auto-logous blood doping might be to insist that athletes intraining take some regular form of marking substancethat shows in the urine, and discontinue it a few daysbefore competition. However, this would be an in-fringement of their rights, and it seems unlikely thatany acceptable method of detection will be developedin the near future.Perhaps the discovery and isolation of erythro-

poetin will make blood doping irrelevant. Erythro-poietin is a direct stimulus to further red cell productionand is a potentially cleaner method of achieving thesame effects. Erythropoietin is not currently a bannedsubstance and the potential for it being used to conferan unfair disadvantage is considerable.We hope that the ethics of sport, particularly Olym-

pic sport, will return to earlier idealistic levels so thatwinning at any medical price, with consequent costlyand constant policing and dope testing become super-seded. The 1988 Olympics were nicknamed the'Anabolic Olympics'. Let us hope the Barcelona Olym-pics do not become the 'Haematocrit Olympics'.

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Bell, J.A., Doege, T.C. Athletes' use and abuse of drugs PhysSportsmed 1987, 15(Mar), 99-108

Berglund, B. Can blood doping be detected? New Stud Ath1988, (suppl) 81-7

Berglund, B., Birgegard, G., Hemmingsson, P. Serumerythropoietin in cross-country skiers Med Sci SportsExerc 1988, 20, 208-9

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tolerance, studies say Phys Sportsmed 1987, 15(Aug),123-7

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Ekblom, B., Goldbarg, A.N., Gullbring, B. Responses toexercise after blood loss and reinfusion J Appl Physiol1972, 33, 157-80

Faulkner, J.A., Kollias, J., Favor, C.B. et al. Maximal aerobiccapacity and running performance at altitute J ApplPhysiol 1968, 24, 685-91

Gollnick, P.D., Armstrong, R.B., Saubert, C.W. et al.Enzyme activity and fiber composition in skeletal mus-cle of untrained and trained men JAppl Physiol 1972, 33,312-9

Hermonsen, L. Oxygen transport during exercise in humansubjects Acta Physiolog Scand 19, 3, 399, 1-104

Holloszy, J.O., Booth, F.W. Biochemical adaptations to en-durance exercise in muscle Annu Rev Physiol 1976, 38,273-91

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Ljungqvist, A. Doping-the wrong way to the top New StudAth 1987, 2, 9-13

Robertson, R.J., Gilcher, R. Metz, K.F. et al. Effect of inducederythrocythaemia on hypoxia tolerance during physi-cal exercise I Appl Physiol 1982, 53, 490-5

Ruska, H. et al. Aerobic performance capacity in athletesEuro J Appl Physiol 1978, 38, 151-9

Smith, M.H., Sharkey, B.J. Altitude training: Who benefits?Phys Sportsmed 1984, 12, 48-62

Thompson, J.M., Stone, J.A., Ginsburg, A.D. et al. 02 trans-port during exercise following blood reinfusion J ApplPhysiol 1982, 53, 1213-9

Tucker, A., Stager, J.M., Cardain, L. Arterial 02 saturationand maximal 02 consumption in moderate-altituderunners exposed to sea level and 3,050m JAMA 1984,252. 2867-2871

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