sports-related flow limitations in the iliac arteries in endurance athletes

This material isthe copyright of theoriginal publisher.

Unauthorised copyingand distribution

is prohibited.

Sports Med 2004; 34 (7): 427-442LEADING ARTICLE 0112-1642/04/0007-0427/$31.00/0

2004 Adis Data Information BV. All rights reserved.

Sports-Related Flow Limitations inthe Iliac Arteries inEndurance AthletesAetiology, Diagnosis, Treatment and Future Developments

Mart H.M. Bender,1 Goof Schep,2 Wouter R. de Vries,3 Adwin R. Hoogeveen2 andPieter F.F. Wijn4

1 Department of Surgery, Maxima Medical Centre, Veldhoven, The Netherlands2 Department of Sportsmedicine, Maxima Medical Centre, Veldhoven, The Netherlands3 Department of Sports Medicine, University Medical Centre, Utrecht, The Netherlands4 Department of Applied Physics, University of Technology, Eindhoven, The Netherlands

Approximately one in five top-level cyclists will develop sports-related flowAbstractlimitations in the iliac arteries. These flow limitations may be caused by a vascularlumen narrowing due to endofibrotic thickening of the intima and/or by kinking ofthe vessels. In some athletes, extreme vessel length contributes to this kinking.Endofibrotic thickening is a result of a repetitive vessel damage due tohaemodynamic and mechanical stress. Atherosclerotic intimal thickening is sel-dom encountered in these young athletes. This type of sports-related flow limita-tion shows no relationship with the classical risk factors for atherosclerosis likesmoking, hypercholesterolaemia or family predisposition for arterial diseases.

The patient’s history is paramount for diagnosis. If an athlete reports typicalclaudication-like complaints in a leg at maximal effort, which disappear quickly atrest, approximately two out of three will have a flow limitation in the iliac artery.In current (sports) medical practice, this diagnosis is often missed, since a vascularcause is not expected in this healthy athletic population. Even if suspected, theroutinely available diagnostic tests often appear insufficient. Definite diagnosiscan be made by a combination of the patient’s history and special designed testsconsisting of a maximal cycle ergometer test with ankle blood pressure measure-ments and/or an echo-Doppler examination with provocative manoeuvres like hipflexion and exercise.

Conservative treatment consists of diminishing or even completely stoppingthe provocative sports activity. If conservative treatment is insufficient or deemedunacceptable, surgical treatment might be considered. As surgery needs to betailored to the underlying lesions, a detailed analysis before surgery is necessary.Standard clinical tests, used for visualising atherosclerotic diseases, are inade-quate to identify and quantify the causes of flow limitations. Echo-Dopplerexamination and magnetic resonance angiography with both flexed and extendedhips have been proven to be adequate tools. In particular, overprojection andeccentric location of the lesions seriously limit the usefulness of a two-dimension-al technique like digital subtraction angiography.

In the early stages, when kinking has not yet led to intimal thickening orexcessive lengthening, simple surgical release of the iliac artery is effective.



is prohibited.

428 Bender et al.

However, for patients with excessive vessel lengths or extensive endofibroticthickening, a vascular reconstruction may be necessary. A major drawback ofthese interventions is that long-term effects and complications are unknown.

As both the diagnostic methods and the treatments for this type of flowlimitation differ substantially from routine vascular procedures, these patientsshould be examined in specialised research centres with appropriate diagnostictools and medical experience.

Approximately one in five top-level cyclists, even a venous graft.[16,17,19,24] However, approxi-triathletes and speed skaters develop sports-related mately two out of three athletes appear to sufferflow limitations in the iliac arteries.[1] In 80% of mainly from functional kinking, which can bethese athletes, the flow limitations increase progres- solved with less invasive surgical techniques.[1]

sively.[2] Therefore, if left untreated, these limita- Since the long-term effects of such extensive vascu-tions will inevitably end the sports career of a sub- lar reconstructions in this young population are stillstantial number of endurance athletes. unknown, less invasive surgery, which leaves the

vessels intact, seems a preferable alternative.[1]Since vascular problems in young and healthyPercutaneous transluminal angioplasty (PTA)athletes are unexpected, one will easily overlook the

and intravascular stents, which have become accept-correct diagnosis. This is illustrated in the literatureed therapies for incapacitating atherosclerotic aorto-since many articles warn against missing this seriousiliac lesions,[25] proved to be ineffective and willsports-related vascular problem.[3-14]

cause substantial risks in athletes with sports-relatedThe history of this sports injury in the medicalvascular injuries in the iliac arteries.[26-29]

literature dates only from 1985 onwards.[4] Cheva-The main objective of this article is to give alier was the first one who suggested an aetiological

practical outline of current knowledge concerningfunctional mechanism in 1986.[5] The researchflow limitations in the iliac arteries in endurancegroup around Chevalier provided more detailed his-athletes. Special attention is given to the most recenttological information in 1990 and introduced thefindings concerning aetiology, prevalence, diagno-term ‘endofibrosis’.[15] The underlying lesions oftensis and treatment.prove to be subtle and located eccentric in the ves-

sel. Therefore, it proves difficult to assess theselesions with conventional vascular diagnostic tools, 1. Aetiologyand also an optimal treatment is not the same as inatherosclerosis.[16-18] In 1997, two important reviews Flow limitations in arteries are most commonlyon endofibrotic lesions were written by the groups caused by atherosclerosis. However, the sports-re-of Chevalier and Abraham.[16,17] In 1999, it was first lated vascular problems encountered in the iliactheorised that functional mechanisms could also arteries in endurance athletes occur predominantlycause flow limitations in the iliac arteries.[19] Diag- in young and healthy athletes who seem to be notnostic tools were developed[19] and subsequently prone for atherosclerosis.[2] These flow limitationsvalidated in more extensive studies.[1,2,20-23] It was seem to be related to specific provocative sportsproved that kinking of the common and/or external activities, such as cycling.iliac artery could give an important contribution to In order to understand the aetiologicalthe flow limitations encountered in these pa- haemodynamic and mechanical stress caused bytients.[1,2,20-23] provocative sports activities, we will give an outline

For athletes with extensive intravascular en- of the anatomy of the iliac arteries and the eventsdofibrotic lesions, the preferred treatment consists that take place during provocative sports and linkof major surgery encompassing a vascular recon- this information to the vascular abnormalities instruction often with the use of a venous patch or these athletes.

2004 Adis Data Information BV. All rights reserved. Sports Med 2004; 34 (7)



is prohibited.

Sports-Related Iliac Artery Flow Limitations 429

1.1 Anatomic Relationships of the during its passage under the inguinal ligament by itsIliac Arteries collateral branches.[31] The number of these collater-

al branches (superior and inferior pudendal artery,superficial circumflex artery and the superficial epi-The iliac arteries are located ventral to the axis ofgastric artery) and their rigid-angled relation to themovement of the hip joint (figure 1). Therefore,arterial trunk may account for this fixation. In con-flexion of the hip induces excessive lengthening intrast, the bifurcation of the common iliac arterythe iliac arteries, which needs to be accommodatedappears normally to be mobile.[30,31] This meansfor by either the natural longitudinal elasticity of thethat, in the normal situation, the physiological vesselvessels or by an increase in tortuosity. Since the iliaclength excess that results during hip flexion will beartery is located upon the psoas muscle, hypertrophyaccommodated by an elastic recoil and increase inof the psoas muscle leads to further ventral displace-tortuosity in both the common iliac artery and thement of the iliac artery (figure 1), which contributesexternal iliac artery, since they behave as one vessel.to a further increase in the physiological excessive

lengthening during hip flexion. When the external1.2 Kinking and Endofibrotic Lesionsiliac artery is tethered to the underlying structures,

the possibilities for this vessel to accommodate forOur group observed extensive adhesions in 18its excessive length during the flexion movement by

out of 23 endurance athletes with iliac artery flowelasticity and mobility may be limited. This willlimitations during operative treatment. These adhe-result in increased tortuosity or even kinking of thesions were encountered especially at the bifurcationvessel.of the common iliac artery and resulted in a fixationNatural fixations of the iliac arteries are bifurca-of the vessel.[1,30,31] Also, fixation of the externaltions (aortic bifurcation, bifurcation of common ili-iliac artery to the psoas muscle by a side branch wasac to external and internal iliac artery and femoralobserved in 50–60% of these athletes.[1,5] Both fixa-bifurcation) and origins of side branches.[30] Cadav-tions may, during hip flexion, disturb the normaler studies show that the femoral artery is fixedphysiological recoil and the normal physiologicalincrease in tortuosity of the iliac arteries. The ves-sels may be tethered and in combination with therelative length excess of the vessel that occurs dur-ing hip flexion a kinking may result.[20,23] Suchkinking results in functional narrowing, which canbe demonstrated by a significant increase in peakblood flow velocity measured with echo-Doppler.[23]

Due to kinking, the blood will collide against thevessel wall with a substantial increased flow veloc-ity.[23] This results in a significant increase in thelocal haemodynamic load on the vessel wall. Even-tually, this increased haemodynamic load may resultin intravascular injury of the endothelium, whichcan provoke an endofibrotic reaction.[5,15,19]

These observations are in accordance with find-ings that about 90% of the endofibrotic lesions arelocated in the external iliac artery, 5% in the com-mon iliac artery and 10% in the femoral artery,while in some cases there are combined le-sions.[16,17,24,32]

Also, in line with the underlying mechanisms arethe histological features of the affected vessels. Mi-

Fig. 1. Oblique view of a three-dimensional image obtained bymagnetic resonance angiography. The image shows the most rele-vant anatomic relations between the iliac arteries, the psoas mus-cles and the hips. It is clearly visible that the iliac arteries arelocated upon the psoas muscle, ventral to the joint axis that runsbetween both hips.


https://www.researchgate.net/publication/11507410_Detection_and_treatment_of_claudication_due_to_functional_iliac_obstruction_in_top_endurance_athletes_A_prospective_study?el=1_x_8&enrichId=rgreq-b7a52af6112ee8d19bb23bb24ace2a76-XXX&enrichSource=Y292ZXJQYWdlOzg0NzQzNDU7QVM6MTAyMTUzNjU4MDQ0NDM2QDE0MDEzNjY3Mzg3MDU=


https://www.researchgate.net/publication/12038405_Pressure_measurements_at_rest_and_after_heavy_exercise_to_detect_moderate_arterial_lesions_in_athletes?el=1_x_8&enrichId=rgreq-b7a52af6112ee8d19bb23bb24ace2a76-XXX&enrichSource=Y292ZXJQYWdlOzg0NzQzNDU7QVM6MTAyMTUzNjU4MDQ0NDM2QDE0MDEzNjY3Mzg3MDU=



is prohibited.

430 Bender et al.

croscopic examination shows a stratified enlarge- Cyclists and coaches often try to improve thement of the intima consisting of moderately cellular cycling efficiency by changing the pedalling tech-connective tissue.[15,24] On electron microscopic ex- nique to increase the pulling forces on the pedals.amination, the cells have characteristics of muscle However, biomechanical studies comparing elite-cells and they can be labelled by anti-actin and anti- national class cyclists with good-state class compet-myosin.[15] These features correspond with a reac- itive cyclists show that extra pulling on pedalstion of the vessel to an extreme haemodynamic load seems to be of no practical use. In contrast to whatin combination with mechanical stress. These en- many coaches and cyclists believe, elite cyclistsdofibrotic characteristics are clearly different from

have optimised their cycling efficiency mainly by aatherosclerosis and fibromuscular dysplasia.[15,33,34]

greater force in downstroke and not by extra pullingon their pedals.[38] In addition, echo-Doppler mea-

1.3 Biomechanical Aspects in Relation to surements in patients with flow limitations in theIliac Artery Flow Limitations iliac arteries show that contractions of the psoas

muscle can lead to a significant increase in iliacartery flow limitations.[23] Thus, pedalling tech-Flow limitations in the iliac arteries of endurance

athletes are related to provocative sports activi- niques that involve extra pulling on the pedals needties.[16,17,19,24,35] Cycling and speed skating are the to be strongly discouraged, because they increasemost significant provocative sports.[19] These activi- the risk of iliac artery flow limitations.ties are characterised by endurance exercise with ahigh demand for blood flow combined with inter-

1.4 Atherosclerosis and Sports-Related Iliacmittent hip flexion. In competition and training, theArtery Flow Limitationsload upon the iliac vessels may be rather extreme.

For example, a professional cyclist cycles approxi-Observational research in 58 cases of sports-mately 35 000km a year. Hip flexion takes place

related iliac artery flow limitations show that there isabout 8 000 000 times a year, while the blood flowthrough the iliac arteries may reach values of about no relationship with well known atherosclerotic risk10 L/min. factors, such as family predisposition, smoking and/

or hypercholesterolaemia.[2] In contrast, since theDuring competitive cycling and speed skating,iliac artery is one of the predilection places fordiminishing the air resistance by optimising the seat

position is paramount. An optimum aerodynamic atherosclerosis, it is even possible that the previous-position is obtained with the back in a horizontal ly described functional mechanisms (kinking) mayposition. This can only be accomplished by in- be (partly) responsible for this preference. Untilcreased hip flexion. Regrettably, this increases the now, no research has been done to question whetherexcessive length in the iliac arteries and will so functional kinking plays a role in flow limitations inincrease the tendency for kinking. Recumbent cy- the iliac arteries due to atherosclerosis. This may becling would diminish this risk, but recumbent cycles caused by the fact that kinking of the arteries in thisare not allowed for competition by the international vessel area is only described from 1999 onwards.[19]

cycling union (UCI).Currently, we have examined some patients with

In the last 20 years there has been a furtherminor atherosclerotic flow limitations in the iliacdevelopment in shoe-pedal connections in competi-arteries, who developed major flow limitations withtive cycling.[36] With a very tight shoe-pedal connec-hip flexion due to kinking (unpublished observa-tion, the recruitment of the leg muscles during cy-tions). Therefore, in patients with atheroscleroticcling changes, and especially the relative contribu-lesions in the iliac arteries who are active in provoc-tion of the flexor muscles to pedallingative sports, further investigation to kinking is indi-increases.[36,37] This may result in hypertrophy of thecated, especially if their complaints increase withpsoas muscle, resulting in a more ventral displace-

ment of the iliac arteries. incremental hip flexion.


https://www.researchgate.net/publication/15028483_Biomechanical_Factors_Associated_with_ShoePedal_Interfaces?el=1_x_8&enrichId=rgreq-b7a52af6112ee8d19bb23bb24ace2a76-XXX&enrichSource=Y292ZXJQYWdlOzg0NzQzNDU7QVM6MTAyMTUzNjU4MDQ0NDM2QDE0MDEzNjY3Mzg3MDU=





is prohibited.


2. Prevalence caused by flow limitations in the iliac arteries. Next,the causative lesion and its exact location should be

From the literature, hardly any data exist on the identified to tailor an optimal treatment strategy.prevalence of flow limitations in the iliac arteries inendurance athletes. These vascular problems were 3.1 Sensitivity and Specificity of Diagnosticoften not recognised, because adequate diagnostic Tools: Confusion Around the Appropriatetools were not available. However, since the popula- Gold Standard for Iliac Arterytion at risk for these abnormalities is well delineated, Flow Limitationsit is possible to obtain some data of the prevalence.

There is confusion in the literature concerningAmong a Dutch group of 25 cyclists andthe efficacy of diagnostic tests for flow limitationstriathletes selected for the Olympic games in 2000,in the iliac arteries. In some publications, a highfive athletes (20%) were previously treated surgical-efficacy for post-exercise ankle to arm index andly for flow limitations in the iliac arteries. In a groupecho-Doppler examination were report-of 35 asymptomatic Dutch national- and internation-ed.[16-18,24,39,40] However, these diagnostic tools wereal-level cyclists, who were examined in 1996 andtested in cyclists, who already underwent a vascular1997, six cyclists (17%) were diagnosed with flowreconstruction or who had clear endofibrotic lesionslimitations in the iliac arteries 5 years later. Bothvisible on digital subtraction angiography (DSA).findings indicate that approximately one in five top-These studies, therefore, only show that these diag-level cyclists will develop iliac artery flow limita-nostic tools were accurate in a population with se-tions. The prevalence for Dutch recreational cyclistsvere flow limitations. However, because patientsis unknown.with minor complaints and minor abnormalitiesChevalier (Lyon, France) performed 223 vascu-were not examined, it is impossible to determine thelar reconstructions on endurance athletes fromreal sensitivity of the applied tools. Studies includ-1985–96.[24] Fifty six percent of these patients wereing both athletes with suspicious leg complaints andyounger than 30 years of age, 15% were profession-control subjects, demonstrate that all currently avail-al cyclists, 48% top amateur cyclists and 28% recre-able diagnostic tests (including post-exercise ankleational cyclists. There were also seven (3%)to arm index and echo Doppler examination) have atriathletes, one (0.5%) cross-country skier (skatingserious lack in diagnostic sensitivity.[2,13,21]

technique) and ten (4.5%) runners. The runners wereCurrently, there is only one study available with-of considerable older age compared with the other

out selection bias and with enough patients thatsubjects.tackles many of the above-mentioned methodologi-Although rowing and speed skating involve en-cal problems.[2,21] In this study, 92 symptomatic legsdurance activity of the legs with intermittent hipwere included from 80 athletes, who were active inflexion, until now no rowers and speed skaters haveendurance sports involving both legs (i.e. >5 hoursbeen described in the literature with flow limitationsper week for more than 3 years). All athletes exper-of the iliac arteries. However, we repeatedly exper-ienced pain, feelings of powerlessness and/or crampienced that in endurance athletes with flow limita-in the leg at maximal effort, which disappearedtions in the iliac arteries, who combine speed skatingquickly at rest. These complaints were not restrictedwith cycling, most complaints develop during speedto a localised area in a single muscle or tendon.skating. We also experienced that speed skaters tendThirty-five asymptomatic cyclists, matched forto attribute their complaints to the specific asymmet-maximal work capacity, served as a control group.ric movement in skating, which will contribute to aRetrospectively, the abnormalities in the legs weresubstantial delay in diagnosing an underlying iliacclassified as vascular or non-vascular, following aartery flow limitation.decision algorithm, based upon the results of diag-nostic tests and treatments over a period of 2 years.3. DiagnosisThis clinical classification could be validated by an

In diagnosing an iliac artery problem in subjects, independent statistical categorisation.[21] In thisfirst one needs to prove whether complaints are group of 92 symptomatic legs, 58 legs (63%) were




is prohibited.

432 Bender et al.

Table I. Relevant diagnostic values of test items to detect flow limitations in the iliac arteries in endurance athletes with claudication-like legcomplaintsa

Test variable Vascular Non-vascular Sensitivity Specificity(n = 58) (n = 34)

Patient’s history

Disappearance of complaints in less than 5 min rest 56 24 0.97 0.29

Calf complaints 20 0 0.34 1.00

Complaints in more than 3 out of 6 muscle areas (buttock, 28 2 0.48 0.94hamstring, adductor, quadriceps, outside upper leg and calf)

No backache 25 8 0.43 0.76

Physical examination

Femoral bruit with extended hip 21 2 0.36 0.94

Femoral bruit with flexed hip 44 12 0.76 0.65

Cycling test

Ankle brachial index <0.54 23 0 0.43 1.00

Ankle difference (unaffected leg-affected leg) >23mm Hg 35 1 0.73 0.95

Echo-Doppler examination

Kinking in the external iliac artery

judgment possible 54 (93%) 30 (88%)

kinking present 21 0 0.39 1.00

Intravascular lesion in the external iliac artery

judgment possible 54 (93%) 30 (88%)

lesion present 33 2 0.61 0.93

a In 80 endurance athletes with claudication-like complaints, 92 legs were categorised as experiencing flow limitations in the iliacarteries or suffering from other causes. No single test on its own combines enough sensitivity with specificity to act as a satisfactorydiagnostic tool. However, application of several tests results in a satisfactory diagnostic tool (for more details, see Schep et al.[2]).

classified as vascular, 29 (32%) as non-vascular and tion to minor back and/or sacro-iliac joint disor-five (5%) as inconclusive. The latter were consid- ders.[21,41] These latter patients often respond well toered non-vascular.[21] In a approximately two out of manual therapy. Therefore, in athletes with morethree vascular patients, kinking of the iliac arteries atypical complaints, manual therapy might be usedwas identified as the major cause of flow limitation. both diagnostically and curatively. However, one

needs to be careful, since more than half of theAfter validation of this categorisation, it provedpatients with flow limitations in the iliac arteriespossible to measure the real diagnostic efficacy ofalso have back complaints and improve partiallyall available tools that were used in this study (seewith manual therapy.[2] Reassessment after manualtable I).therapy remains necessary, combined with instruc-tions to return if the complaints have not disap-3.1.1 Patient’s History and Physical Examinationpeared completely.In a setting with no additional test facilities, one

has to rely on the patient’s history and a physical In physical examination, ankle pressure measure-examination to select patients who need further test- ments at rest or palpation of pedal pulses is almosting. If endurance athletes complain of “pain, loss of never of any use, since the flow limitations are sopower and/or a cramp at maximal effort, which subtle. These tests will only be abnormal in the veryaffect multiple muscles and is not restricted to a severe cases or in cases with a complete occlusionlocalised area in a muscle or in a tendon” and when due to arterial thrombosis or intimal dissection. Aus-these complaints disappear quickly at rest, 60% of cultation of the iliac artery at rest is helpful inthem prove to experience a flow limitation in the patients with minor iliac artery flow limitations.iliac arteries.[21] Other important causes of such With the hips extended this proves quite specific andcomplaints are pseudo-radicular syndromes in rela- with the hips flexed it is most sensitive. After exer-




is prohibited.


cise, however, auscultation of the iliac artery is of no recovery they obtained a sensitivity of 90% and ause, as also in most normal reference subjects a specificity of 86%. This diagnostic accuracy couldfemoral bruit is audible. be improved slightly by using the ankle brachial

Table I summarises the diagnostic efficiency of index to heart rate relationship in the first minute. Inthe most important test-items from patient’s history 11 patients (14%) they were unable to give a definiteand physical examination. diagnosis and these were excluded from their analy-

sis resulting in some overestimation of the computed3.1.2 Cycle Ergometer Test with Ankle Blooddiagnostic accuracy.Pressure Measurement

Provocative cycle tests can be used in both sports Both previous research reports included patientsmedicine facilities and vascular laboratories. This who had proven iliac artery endofibrosis. Patientsserves as one of the most practical and concise with suspected complaints, but without proven en-diagnostic tools to demonstrate a flow limitation and dofibrosis, were excluded from the study of Fernan-it can also be helpful in grading the extent of such dez-Garcia et al.[39] and in the study of Abraham etflow limitation. Already in 1986, both Mosiman et al.,[40] which results in overestimation of the diag-al.[4] and Chevalier et al.[5] described the diagnostic nostic accuracy.value of the cycling test. More recently, one tried to

Taylor et al.[13] demonstrated this difficulty in 12assess and improve its diagnostic value.[13,39,40,42]

patients with suspected leg complaints. Only threeDesvaux et al.[42] determined normal values of anklemet his diagnostic criterion of an ankle brachialbrachial indexes of 0.75 ± 0.09 in 15 healthy sub-index under 0.50. In these three subjects, and injects after maximal exercise and they demonstratedanother one that had a difference between healthya gradual drop in ankle brachial index from submax-and affected leg of above 0.18, he could demonstrateimal exercise to maximal exercise. Next, theyiliac artery endofibrosis. The diagnosis in the otherdemonstrated that trained athletes had somewhateight athletes remained uncertain and points to thehigher ankle brachial indexes compared with un-lack of a gold standard in these patients (see sectiontrained subjects (0.80 ± 0.08 vs 0.70 ± 0.06, respec-3.1). The observations of Taylor et al.[13] are in linetively).[43] In general, a slight rise in pressures dur-with our findings. However, by adapting our mea-ing the first minute after exercise was observed,suring procedure, we could gain substantially on thefollowed by a gradual drop. Also, the arm pressuressensitivity of this test.[19,21] Immediately after exer-seem to drop faster than the leg pressures. Suchcise, we perform simultaneously automated bloodpatterns underline the necessity of simultaneouspressure measurements at both ankles and arms asmeasurements of the pressures in the arm and infast as possible in a position with the hips flex-both legs.[13,39,40,42] The reported normal values wereed.[19,21] This measurement can be performed lyingconfirmed by other researchers.[13,39,40,42]

supine on a bench with the hips flexed, or even at theFernandez-Garcia et al.[39] claimed a diagnosticbicycle, using a support for the feet to maintain aaccuracy of around 1.00, when comparing patientscomparable flexed position in both hips. The firstwith confirmed endofibrosis and healthy adults.measurements (most often after 30–60 seconds) areHowever, these authors used a subset of patientsused as a main diagnostic criterion, and the timewith severe lesions and in doing so are overestimat-course is followed by monitoring the pressure differ-ing the sensitivity.ences in the following minutes. It is essential thatAbraham et al.[40] performed a well designedone corrects the ankle pressures for the height differ-study. They compared 38 patients with confirmedence between ankle and arm (1cm = 0.76mm Hg).external iliac artery endofibrosis with 118 healthyComparing blood pressure differences in four pa-subjects and 40 patients with leg complaints that intients and five reference subjects with flexed andfollow-up proved to be of non-vascular origin. Theyextended hips we observed in the reference subjectstried to asses the best possible diagnostic criterionno changes in pressure difference, in contrast to theand compared different minute intervals of pressurepatients who showed a substantial increase in themeasurements after exercise. Using a brachial index

value of 0.66 measured after the first minute of affected legs (unpublished observations).




is prohibited.

434 Bender et al.

Using this way of testing, it is possible to confirma flow limitation in a substantial number of patients,however, sensitivity is still not optimal. If there is ahealthy leg to compare with, the sensitivity amounts73% with a specificity of 95%. Approximately 20%of the patients experience symptoms in both legs,and in these patients one has to rely on the anklebrachial index, which has a sensitivity of only 43%with a specificity of 1.[2] The diagnostic efficiencyof this test is summarised in table I.

Kinking

Fig. 2. Echo-Doppler images of the external iliac artery; left: apatient diagnosed with a flow limitation in the external iliac artery ina body position with the hips extended. Note that the iliac arteryruns a straight course and that there is no kinking; right: the samepatient with his hips flexed, approximately 120°. Note that kinking isprovoked (arrow).

3.1.3 Echo-Doppler ExaminationEcho-Doppler examination is able to produce an longer follow-up and to repeat the diagnostic tests if

image of the underlying lesions and is, therefore, the complaints aggravate in time.also of importance in making decisions for optimal

3.2 Visualisation and Grading of the Causestreatment. Hence, its application should be linked toof Flow Limitationclinical settings in which specific surgical treat-

ments can be performed. An echo-Doppler examina-If a flow limitation in the iliac artery is detected,tion is not invasive and can therefore also be applied

the next question is: which treatment is most suita-as a first-line diagnostic tool. However, there is able? Since the complaints and lesions are progres-considerable learning curve to score the lesionssive in almost 80% of patients, some action isproperly and the imaging quality is sometimes notmandatory for almost all patients. Although it isenough to do reliable scoring. See table I for thepossible to accept the handicap and change thediagnostic efficiency.[23]

sports activity (e.g. stop cycling and start swimming3.1.4 Combination of Tests or running), this will rarely be acceptable for most

professional cyclists, and even recreational sport-The combined information of patient’s history,speople are most often eager to continue their sports.physical examination, a provocative cycling test,Consequently, in a substantial number of patients,and echo-Doppler examination gives very high ac-further treatment needs to be considered.curacy for diagnosing flow limitations in the iliac

To define an optimal treatment, it is necessary toarteries, with a sensitivity and specificity overvisualise and scale the underlying mechanisms of0.90.[2] Nevertheless, a small subgroup of patients,flow limitations, such as kinking and/or stenoticespecially those who experience kinking in the com-lesions of the vessels.[1,5,19,20,22,23] These abnormali-mon iliac artery, may at an early stage of theirties are mainly observed in the common iliac arterydisease still become misdiagnosed as non-vascular.and/or the external iliac artery. More rarely abnor-This is due to the limited capacities to detect kinkingmalities are encountered in the femoral arteries,in the common iliac artery by echo-Doppler, sinceeven after the femoral bifurcation.[32] Kinking ofthese kinkings are predominantly in the frontalthese arteries during hip flexion may be caused byplane, which is not easily visualised with echo-fixations due to a side branch at the psoas muscle, byDoppler[20,23] (see figure 2). Misdiagnosis may alsotight fibrous tissue, especially at the iliac bifurca-occur due to the fact that ankle pressures after exer-tion[1] or by excessive lengths of the arteries.[22]cise return rapidly to normal, once the kinking is

diminished in the recovery period. Therefore, if the Kinking due to fixation can effectively be treatedresults of the provocative cycling test and the echo- by surgical release of the iliac artery, leaving theDoppler examination are normal,[20,21] one may add vessels intact (see section 4.2). This diminishes themagnetic resonance angiography (MRA) with the risk for long-term complications.[1] If kinking iships flexed. If all tests are normal and patients still caused by excessive vascular length or if a vascularremain clinically suspect of a flow limitation in the stenosis is responsible for the flow limitation, sim-iliac arteries, it is desirable to give these patients a ple surgical release will not suffice and a vascular







is prohibited.


reconstruction might be warranted, with risks forpotential long-term complications.[1,16,17,24] If oneunderestimates the severity of the lesions and justperforms surgical release, the resulting tissue scar-ring will complicate a subsequent vascular recon-struction when necessary. Therefore, to determinethe most optimal treatment, a detailed assessment ofthe extent and location of the underlying lesions iscrucial.

3.2.1 KinkingKinking in the external iliac artery can best be

detected with echo-Doppler examination combinedwith hip flexion, with psoas contraction and afterexercise [23] (see figure 2). Doppler measurementssupport evidence for kinking, especially if the peak

Fig. 3. Images of the aorto-iliac tree obtained with magneticresonance angiography with flexed hips. Both images are position-ed to obtain approximately the same orientation (an oblique posteri-or view of the arteries with the left artery on the left side). Left: areference subject with arteries that run smoothly and straight.Right: a patient with left-sided iliac artery flow limitations. Note thesevere kinking that is visible in the proximal common iliac artery(arrow).

systolic velocity increases with flexed hips com-pared with extended hips, and with isometric psoas distance are possible[22] (see figure 4 and table II).contraction. The kinks in the iliac artery prove most To estimate whether surgical release of the iliacoften to be in a sagittal plane and can therefore be arteries may be feasible, reference values may bevisualised in the most appropriate plane using echo- used. In doing so, one has to realise that furtherDoppler. The arterial pulse wave attenuates kinking, prospective studies are necessary to define the exactwhich makes it easier to identify kinking with real- maximal vessel length, which still allows benefittime visualisation. In 40% of patients with iliac from surgical release.[22] Only a small number ofartery flow limitations, kinking in the external iliac patients proves to be characterised by extreme ex-artery can be detected, while such kinking was not cessive vessel lengths, and approximately 90% ofobserved in any of 28 reference legs.[23] In contrast, patients have vessel lengths in the normal range.[23]

MRA is less effective, since imaging can be made at3.2.3 Intravascular Lesionsrest only, providing a static image without the dy-In conventional vascular medicine, lumen diame-namic real-time visualisation of the pulse wave.[20]

ter reductions to 50% or more are considered clini-Kinking in the common iliac artery can best becally significant. All imaging techniques are testedvisualised by MRA with the hips flexed[20,23] (seeand designed to have the optimal diagnostic accura-figure 3). For reliable detection, 3-dimensional scor-cy in this area of interest.[44-46] However, for flowing of the vessels and proper positioning of thelimitations in the iliac arteries, the threshold to de-suspected kinking in the exact plane of reference arecide between treatment with vascular reconstructionessential.[20] In 48% of athletes with iliac artery flowor a less invasive surgical release is around diameterlimitations, kinking in the common iliac artery canreductions of 10–30%.[1] Currently, a more exactbe detected, while such kinking was only observedthreshold is not available, since at the time of thein one of 32 reference legs (3%).[9] Echo-Dopplerrelevant study[1] the scoring methods of these in-examination of this kinking appears very difficult,travascular lesions were subjective and more or lessbecause such kinking is most often located in theinaccurate.frontal plane, which cannot be visualised in an ap-

Most endofibrotic lesions are located eccentric inpropriate way.[20,23]

the vessel wall, which necessitates that one visual-3.2.2 Length of the Arteries ises the vessel from the most accurate plane. SinceExcessive length of the arteries can best be as- most lesions are also located near to the iliac bifur-

sessed using MRA with the hips extended. Exact cation in the proximal part of the external iliacmeasurements of the respective vessels and calcula- artery, this especially limits the use of DSA due totion of the ratios of vessel length to straight-line overprojection of bone and other vessels. Conse-








is prohibited.

436 Bender et al.

25%, Doppler measurements lack sufficient dis-criminative power.[23,44-46]

MRA has considerable advantages, since it is athree-dimensional technique. Contrast-enhancedimages can be made with a spatial resolution ofapproximately 3mm3 that gives sufficient accuracyin the relevant diagnostic range.[22] Digital post-processing of vessel tracking with measurements ofvessel diameters and surfaces on every location inthe artery is technically possible (see section 3.2.2),and may tackle the problems of eccentric lesions andoverprojection of other vessels.[22] However, the ar-terial pulse wave may induce relatively large vesselmovements, which may obscure detection of dis-crete intravascular lesions by MRA, because rela-tively long illumination times (about 90 seconds) areused. This sort of artefact may especially be dis-turbing in this group of patients. Using echo-Dop-pler, we measured in 58 patients with flow limita-tions vessel movements of 3.0 ± 1.2mm (mean ±SD) [unpublished observations].

For imaging of intravascular lesions in currentpractice, we advise the use of a combination ofecho-Doppler and MRA. In patients in whom arteri-

Fig. 4. Images of the aorto-iliac tree obtained with magneticresonance angiography. Top: the aorto-iliac tree in a referencesubject. Bottom: the aorto-iliac tree of a patient with excessivevessel lengths. Both subjects were <35 years of age and had norisk factors for atherosclerosis and/or hypertension. The images onthe left and in the middle are obtained with the hips extended, andthe images on the right with the hips flexed. Note the excessivevessel lengths in the patient, which result in kinking of both thecommon iliac artery on the left side and of the external iliac arteryon the right side with hip flexion (arrows). al pulse-wave-related vessel movements are ob-

served in excess of 2mm, MRA may underestimatequently, DSA typically underestimates these eccen- the lesions. When interpreting the MRA findingstric endofibrotic lesions. using the information obtained with echo-Doppler,

The use of the echo-Doppler technique may be one becomes aware of possible movement artifactslimited by problems in image quality. Also, with in the MRA and one has the opportunity to defineecho-Doppler it is not possible to visualise the ves- the vessel areas that may have imaging artifacts duesels from all angles, which limits the detection of the to vessel movement. Cardiac-triggered MRA mayeccentric endofibrotic lesions. Doppler measure- potentially lessen this problem in the near future.ments give additional functional information. How- DSA may also be useful in the more extreme cases,ever, for scoring of lesions in the diagnostically because of its relatively short illumination time.interesting range of diameter reductions around Cineangiography (which is routine in cardiac

Table II. Measurement of actual vessel lengths and straight line distances of the vessels from figure 4 using post-processing techniques[22]a

Common iliac artery External iliac artery

hips extended hips flexed hips extended hips flexed

left right left right left right left right

Reference subject 1.04 1.02 1.09 1.08 1.09 1.04 1.26 1.34

Patient 1.36 1.25 1.33 1.22 1.16 1.33 1.46 1.73

Reference values 1.05 ± 0.04 1.11 ± 0.05 1.08 ± 0.05 1.32 ± 0.13(n = 32)

a The ratio between vessel length and straight line distance is a measure of excessive length. These ratios are assessed for bothsubjects. The results can be compared with reference values (mean ± SD) obtained by a group of 16 healthy subjects (= 32vessels, since left and right proved to be not significantly different in reference subjects).




is prohibited.


catheterisation) is especially helpful since it also high prevalence (approximately 20% in cyclists)visualises the vessel movement. When using DSA, and a long period from onset of complaints to finalone needs to be aware that only the original images diagnosis.can be judged, and that post-processing, encompass- Simple screening consists of direct questioninging the adding of images to one another, may lead to about specific leg complaints: pain, loss of powermovement artifacts and diagnostic inaccuracies. and/or cramp at maximal exercise rapidly disappear-

Although nowadays a combination of techniques ing at rest, combined with physical examination ofenables sufficient detailed information to scale in- vascular bruits over the femoral artery with the hipstravascular lesions, a major drawback is the lack of extended and flexed. Such screening is advised dur-knowledge concerning the clinically meaningful di- ing pre-season screening of cyclists, speed skaters,agnostic thresholds. Further research is necessary to cross-country skiers and athletes involved indefine the threshold values of intravascular lesions skeelering. Given the high prevalence of the prob-that are still amenable for surgical mobilisation on- lem and the advantages of early detection, earlyly. application of more sophisticated diagnostic tests

including provocative cycling tests, echo-Dopplerexamination and MRA may be cost effective for3.3 The Importance for Early Detectionnational level and professional athletes.of Patients

4. TreatmentThe diagnosis of flow limitations in the iliac

arteries is often delayed. In our studies, the period There are several treatment options for flow limi-between the onset of symptoms and diagnosis was tations in the iliac arteries. To determine the moston average 3.4 years or 55 000km cycling![1] This is optimal treatment, it is important to consider notin line with experiences of other physicians with only the underlying lesions, but also the situation ofspecial expertise in this area of medicine, like Chev- the patient. Restrictions of the patients due to flowalier.[24] Over time, 80% of these patients experience limitations depend not only on the severity of theprogression of their complaints.[2] It is very likely underlying lesions, but also on the patient’s de-that intravascular lesions gradually worsen if the mands. A professional cyclist advised to stop cy-provocative sports activities are continued. A seri- cling, is rendered jobless. In contrast, alternativeous complication of these endofibrotic lesions con- sports activities may be quite acceptable for a recre-sists of acute occlusion due to either dissection or ational cyclist. In between are the cyclists for whomarterial thrombosis,[3,6,10,16,24] highlighting the dan- cycling has a prominent place in their social life.ger of these lesions. They often cycle in excess of 10 hours a week, and

Optimal treatment depends on the stage of the most of their social life has been centred on sportsdisease. Only athletes with mild structural intravas- for many years. To stop cycling may have an unde-cular lesions are candidates for surgical release of sirable impact on their life. Decisions for an optimalthe iliac arteries. In our series, 40% of patients treatment should also take the lifestyle in considera-already had vascular lesions too extensive for simple tion, and physicians should not only weigh the tech-surgical release.[1] Moreover, half of the patients that nical, but also the social and psychological implica-were treated with surgical mobilisation had still tions of their decisions.some detectable minor residual flow limitations, due The extent of intravascular damage is one of theto remaining intravascular lesions that were left most important factors to determine the most opti-untreated. mal treatment. However, as described in section

Given the progressive nature of the disease, it is 3.2.3, especially in the most relevant range ofessential that physicians, who treat endurance ath- 10–30% diameter reduction, many currently availa-letes, are well aware of possible flow limitations in ble diagnostic imaging tools have limited accuracy.the iliac arteries. They should try to make a definite Moreover, the threshold values of vessel abnormali-diagnosis as soon as possible. There seems to be ties that can still be left untreated without causingample possibilities for optimisation, because of a significant complaints are unknown. Therefore, a






is prohibited.

438 Bender et al.

continuous evaluation of the existing knowledge ureters, iliac veins and nerves. Video enhancementand ongoing research is paramount to make the most may enable a safe meticulous dissection in theseoptimal decisions. areas.

To avoid the recurrence of unfavourable fixation4.1 Conservative Treatment by scar tissue postoperatively, patients are instructed

to restrict endurance exercises with intermittent hipConservative treatment should be the first line of flexions. Activities such as walking and short bouts

treatment. This encompasses the advice to reduce or of low-intensity cycling in an upright position arestop provocative activities. Cyclists can be advised allowed for the first 6 weeks. After a period of 6to change their cycling position in order to decrease weeks, the patients have no further restrictions.hip flexion, not to actively pull the pedal upwards,

Until now, surgical release of the iliac vesselsand to reduce the hours spent on a racing bike. Even

was performed without major complications andwith these measures, cyclists often continue to expe-

with good short-term results. All patients who un-rience complaints, and the disease may still pro-

derwent this intervention improved significantly.gress. Therefore, a change to other sports like run-

Satisfactory return to competition was achieved inning or cycling with a recumbent cycle may be a

20 out of 23 patients,[2] highlighting the necessity ofbetter alternative. Although no follow-up data are

a careful patient selection. Three patients were re-known from the literature, it is reasonable to assume

operated for residual flow limitations, due to in-that such measures may stop further progression of

travascular lesions that were underestimated pre-the abnormalities.[24] However, regression of an ex-

operatively. During reoperation, we noted fixationsistent lesion is not expected, given the histological

of the iliac arteries due to scar tissue of the previousfeatures of the endofibrotic lesions and the nature of

operation; however, this did not lead to recurrentother causative abnormalities, such as excessive

kinking.vessel lengths, adhesions due to psoas side branches,

Theoretically, it is possible that the problem ofor fibrosis.[15,19,22,24] If conservative treatment is notkinking might return after surgical release of thefeasible, further diagnostic imaging needs to beiliac arteries. Follow-up studies are therefore stilldone to determine the optimal surgical option.mandatory. We treated several professional cyclistswith surgical release only. Preoperatively they had4.2 Surgical Release of the Iliac Arteriesprogressive complaints, which if left untreatedwould inevitably result in the end of their career.Surgical release of the iliac arteries, which isPostoperatively, they continued cycling as profes-aimed to solve kinking of vessels during hip flexion,sionals for more than 5 years without progression ofinvolves a minor intervention in which the vesselscomplaints.themselves are left intact. Through an inguinal inci-

sion (4cm wide parallel to and 4cm cranial of the Only when kinking has not led to substantialinguinal ligament) the iliac artery is released from intimal thickening, a surgical release will suffice. Inthe vascular sheath and the underlying surface under a prospective study on surgical release of the iliacvideo enhancement. The release is done predomi- arteries, a lumen diameter reduction to 75% or lessnantly by blunt preparation with limited sharp dis- of the normal diameter served as an exclusion crite-section. If present, psoas branches are ligated and rion.[1] However, the scoring of vessel abnormalitiestransected. In particular, the iliac bifurcation often at the time of this study was rather subjective and anproves to be fixed by tissue which appears as scar accurate measurement of diameter reductions wastissue to surrounding tissue, in contrast to findings not possible.[1] Currently, we have experience thatobserved during cadaver studies in which this bifur- vessels with a diameter of ≤70% compared withcation is rather mobile.[2,30,31] If kinking occurs at the unaffected vessels will not benefit enough from alevel of the common iliac artery, it is necessary to surgical release, whereas for vessels with a diametermobilise the common iliac artery completely up to of ≥90%, surgical mobilisation is most likely to bethe aortic bifurcation. Great care needs to be taken effective. If diameters are reduced to values betweennot to damage the surrounding structures, like 70% and 90%, there is doubt concerning the most




is prohibited.


4.3.2 Endarteriectomy and Closure with a Venousoptimal treatment. Unfortunately, approximatelyPatch and Venous Graft70% of patients have intravascular lesions in thisTraditional therapy for flow limitations in therange, underlining the necessity for further prospec-

iliac arteries is based upon treatment of intravasculartive study.lesions. This consists of surgical mobilisation of theiliac arteries, combined with vascular reconstruction

4.3 Vascular Reconstructions with either endarteriectomy or complete replace-ment by a venous graft.[5,16,17,24,32] Chevalier etal.[16,17,24,32] documented an excellent result in 223Vascular reconstructions are major surgical inter-patients, including return to a high level of competi-ventions with acute risks for damaging vital struc-tion. As these patients were predominantly athletestures during the operation. Intimal hyperplasia in theunder 30 years of age,[16,17,24,32] long-term prognosisoperated artery precludes the use of prosthetic mate-is of paramount importance. However, until now, norial.follow-up data are available but it is not reassuring

In the long run, complications such as aneurysmsthat disappointing long-term results were reported in

at the location of a vein patch and progressive steno- patients who received coronary artery bypass graft-sis at the suture lines in vein grafts remain possible. ing with venous grafts due to sclerosis of these graftsIt is also possible that kinking of the arteries will be and progressive intimal proliferation.[47] Fitzgibbonprovoked by either scarring or by the changes in et al.[47] reported an occlusion rate of 19% after 1vessel stiffness at the ends of the reconstructions. At year, 25% after 5 years and 50% after 15 years.present time, no data are available on the long-term After 15 years, 81% of the remaining open graftseffects. Therefore, if possible, surgery should be showed significant stenoses.avoided and if necessary, the most minimal inter- Despite these risks, with a diameter reductionvention should be applied. greater than 50% or the presence of acute thrombo-

sis or dissection, severe complaints may develop in4.3.1 Shortening of the Vessel daily life, warranting a vascular reconstruction. Al-In some patients, excessive vessel length causes so, professional cyclists with vascular abnormalities

not amenable for less invasive surgery often choosekinking during hip flexion.[22] In such cases, surgicaltreatment with more extensive vascular reconstruc-release has to be combined with vessel shortening.tions, weighing the risks of the intervention againstAlthough reference values are available, there arethe drawbacks of ending their sports career.currently no data available concerning vessel

lengths that are still tolerated without complaints. It4.4 Percutaneous Transluminal Angioplastyappears that at least 80% of patients have vesseland Vascular Stentinglengths in the normal range, while patients who do

not fit the normal range often have extreme vesselPTA and treatment with stents are accepted ther-lengths.[22] During surgery, the iliac vessel is tran-

apies for incapacitating atherosclerotic aorto-iliacsected at the iliac bifurcation at an angle of 45º. The

lesions.[25] The temptation to use these less invasiveexternal iliac artery is shortened and intimal thicken-

procedures in young and active sports people ising at this side is treated by eversion endarteriecto- high.[25] However, the lesion in endofibrosis is en-my, as most of the intravascular lesions prove to be tirely different from an atherosclerotic lesion. En-in the proximal part of the external iliac ar- dofibrotic lesions consist of an asymmetrical intimaltery.[15,23,24]

thickening,[15] are elastic, and recoil in a few daysA suture line at the iliac bifurcation diminishes after PTA.[15,24] There is one case report that de-

the risk for kinking at this suture. Moreover, the 45º scribes short-term relief in an Olympian female ath-angle of the suture line minimises the risk of steno- lete, who was treated with PTA. Although the ef-sis, caused by scar retraction. Since artificial arterial fects of PTA lasted a few weeks and enabled aor venous graft materials are not applied, the risks successful Olympic competition, symptoms re-for long-term complications seem to be low. turned 6 weeks later.[48] Disappointing results of







is prohibited.

440 Bender et al.

PTA are reported in a few cases.[26,27] PTA might be surements after exercise. Research is currently un-a harmful procedure as it increases the risk for derway to test this hypothesis.dissection of endofibrotic lesions.[26,27,29] Since there With imaging techniques like echo-Doppler andare no studies that substantiate any positive long- MRA, it is possible to visualise the underlying le-term effect of PTA on endofibrotic lesions, we ad- sions and mechanisms in sufficient detail. However,vise to refrain from PTA. only a limited number of data are available that link

Vascular stenting is contraindicated. As men- the extent of vessel abnormalities to the effects oftioned earlier, a professional cyclist flexes the hip different treatments. Therefore, further studies needaround 8 000 000 times a year, while during cycling to be done to determine discriminating thresholds8–10L of blood may pass through each iliac artery for different treatment options. As long-term effectsper minute.[19] At every hip flexion, this would result for almost all treatment options are not available,in a relative excessive length in the iliac arteries, prospective studies need to be performed to guidewhich will predispose the vessels to kinking at the optimal treatments in these specific patients, whoends of the stents. The risk of intimal hyperplasia normally still have a long lifespan to go.due to such extreme mechanical stresses is relativelyhigh. To the best of our knowledge, no studies report 6. Conclusionsa positive effect of stenting in endurance athleteswith iliac artery flow limitations. On the contrary, Although recent experience has substantially in-two patients have been referred to us with intimal creased our knowledge concerning sports-relatedhyperplasia due to stenting, and Ruurda et al.[26] also iliac artery flow limitations, this diagnosis is oftendescribe such a case. missed in current medical practice, and consequent-

ly proper diagnostic tests are not widely applied.5. Future Developments and ResearchAlthough it is often possible to obtain a definitediagnosis with proper diagnostic techniques (espe-Since the available epidemiological data indicatecially if the information from different tests is com-a relatively high prevalence of iliac artery flowbined), one still has to be aware that all tests lacklimitations (about 20% in top cyclists), future stud-diagnostic sensitivity. Therefore, if there is suspi-ies on the prevalence in recreational cyclists andcion for an iliac artery flow limitation, one has to beother athletes, such as speed skaters and rowers, areaware that it is very difficult to exclude this diagno-necessary.sis, and a longer follow-up and/or a repetition ofCurrently, it is possible to make a reliable diag-tests after progression of symptoms may be necessa-nosis using a decision algorithm or a combination ofry.provocative tests.[2,21] However, this procedure is

Treatment of these sports-related flow limitationscomplex and time consuming. Since leg complaintsis dependent upon a detailed analysis of the underly-are quite common in endurance athletes, optimisa-ing vascular problems (kinking, excessive vesseltion of the diagnostic techniques is warranted. Ideal-length and/or intravascular narrowing), which arely, a diagnostic tool that gives an instant answer topredominantly located in the common and/or exter-the question whether leg complaints are caused bynal iliac artery.arterial flow limitation or not should be available.

Therefore, the efficacy of the cycling test should be Although it is now technically possible to visual-increased. Currently, it is possible to perform pedal ise these underlying lesions in sufficient detail, theforce measurements during cycling (at the time of exact discriminating thresholds for abnormalitiescomplaints),[19,49,50] and to obtain information on that define the most optimal treatments are not avail-muscle oxygenation in the legs, using near infrared able and long-term effects are unknown for almostspectroscopy.[51] Since both techniques measure all current treatments. Therefore, it is advisable tophysiological phenomena, which are related to flow restrict the treatment of these vascular lesions tolimitations in the iliac arteries during exercise, these specialised centres that have ample experience, themeasurements might increase the diagnostic value right equipment and a structured research setting forof the current cycling test with blood pressure mea- these patients.




is prohibited.


19. Schep G, Bender MH, Kaandorp D, et al. Flow limitations in theAcknowledgementsiliac arteries in endurance athletes: current knowledge anddirections for the future. Int J Sports Med 1999; 20: 421-8

20. Schep G, Kaandorp DW, Bender MH, et al. Magnetic resonanceThe authors are not aware of any conflict of interest that isangiography used to detect kinking in the iliac arteries indirectly relevant to the contents of this review. No sources ofendurance athletes with claudication. Physiol Meas 2001; 22:

funding were used to assist in the preparation of this review. 475-8721. Schep G, Schmikli SL, Bender MH, et al. Recognising vascular

causes of leg complaints in endurance athletes: part 1. Valida-tion of a decision algorithm. Int J Sports Med 2002; 23: 313-21References

22. Schep G, Kaandorp DW, Bender MH, et al. Excessive length of1. Schep G, Bender MH, van de Tempel G, et al. Detection andiliac arteries in athletes with flow limitations measured bytreatment of claudication due to functional iliac obstruction inmagnetic resonance angiography. Med Sci Sports Exerc 2002;top endurance athletes: a prospective study. Lancet 2002; 359:34: 385-93466-73

23. Schep G, Bender MH, Schmikli SL, et al. Color Doppler used to2. Schep G, Bender MH, Schmikli SL, et al. Recognising vasculardetect kinking and intravascular lesions in the iliac arteries incauses of leg complaints in endurance athletes: part 2. Theendurance athletes with claudication. Eur J Ultrasound 2001;value of patient history, physical examination, cycling exercise14: 129-40test and echo-Doppler examination. Int J Sports Med 2002; 23:

24. Chevalier JM. Pathologie vasculaire du cyclistes [in French].322-8Encyclop Med Chir 1997; A10: 11-6753. Cook PS, Erdoes LS, Selzer PM, et al. Dissection of the external

25. Bosch JL, Hunink MG. Meta analysis of the results of percuta-iliac artery in highly trained athletes. J Vasc Surg 1995; 22:neous transluminal angioplasty and stent placement for173-7aortoiliac occlusive disease. Radiology 1997; 204: 87-964. Mosiman R, Walder J, van Melle G. Stenotic intimal thickening

26. Ruurda JP, Rijbroek A, Vermeulen EG, et al. Arterial insuffi-of the external iliac artery: illness of the competition cyclist?ciency in athletes due to ‘endofibrosis’ [in Dutch]. NedReport of two cases. Vasc Surg 1985; 19: 258-63Tijdschr Heelkd 2000; 9: 124-65. Chevalier JM, Enon B, Walder J, et al. Endofibrosis of the

external iliac artery in bicycle racers: an unrecognized patho- 27. Schep G, Bender MH. Comment on the article: ‘arterial insuffi-logical state. Ann Vasc Surg 1986; 1: 297-303 ciency in athletes due to endofibrosis’ [in Dutch]. Ned Tijdschr

Heelkd 2000; 9: 127-86. Del Gallo G, Plisonnier D, Planet M, et al. Dissecting aneurysmof the external iliac artery: an unusual course of endofibrosis in 28. Bradshaw C. Exercise related lower leg pain: vascular. Med Scian athlete [in French]. J Mal Vasc 1996; 21: 95-7 Sports Exerc 2000, S36

7. Pils K, Bochdansky TH, Jantsch HS, et al. Intermittent leg 29. Schep G, Bender MH. Letter to the MSSE editor concerningischemia during competition cycling. Lancet 1990; 336: 189 exercise-related lower leg pain-vascular. Med Sci Sports Exerc

8. Monti M, Jaeger M, Guisan Y, et al. Diagnostic de l’insuffi- 2000; 32: 1970-1cance arterielle peripherique chez le sportif amateur claudicant 30. von Hayek H. Das Verhalten der Arterien bei beugung deret clepistage (syndrome de la stenose arterielle iliaque isolee Gelenke (the movement of arteries when bending joints). Zchez le jeune cycliste sans facteur de risque) due par examen Anat Entwicklungsgesch 1935; 105: 25-36doppler et test sur tapis roulant. Rev Med Suisse Romande 31. Lopez J-F, Magne J-L, Champetier J. The femoral artery and1984; 104: 823-30 flexion of the hip joint. Surg Radiol Anat 1989; 11: 275-81

9. Pillet J, Enon B, Reigne B, et al. La plicature de l’artere 32. Chevalier JM, L’Hoste PM, Bouvat E, et al. L’endofibrosefemorale commune: un diagnostic differentiel de l’endofibrose arterielle du sportif de haut niveau: formes inhabituelles. Jde l’artere iliaque externe du coureur cycliste. J Chir (Paris) Traumatol Sport 1991; 8: 176-811992; 129: 512-3

33. Luscher TF, Lie JT, Stanson AW, et al. Arterial fibromuscular10. Scheerlinck TAM, van den Brande P. Post-traumatic intima dysplasia. Mayo Clin Proc 1987; 62: 931-52dissection and thrombosis of the external iliac artery in a34. Stary HC, Chandler AB, Glagov S, et al. A definition of initial,sportsman. Eur J Vasc Surg 1994; 8: 645-7

fatty streak, and intermediate lesions of atherosclerosis. Amer-11. Schep G, Sala HAGM, Bruyninckx CMA. Leg complaints inican Heart Association. Arterioscler Thromb 1994; 14: 840-56cyclists, description of a relatively unknown occupational dis-

35. Foster C, Rundell KW, Snyder AC, et al. Evidence for restrictedease [in Dutch]. Geneeskunde Sport 1995; 27: 182-4muscle blood flow during speed skating. Med Sci Sports Exerc12. Wille J, De Jong JR, Moll FL, et al. Endofibrosis of the external1999; 31: 1433-40iliac artery in sportsmen clinical review and four new cases.

36. Gregor RJ, Wheeler JB. Biomechanical factors associated withVasc Surg 1998; 32: 323-8shoe/pedal interfaces: implications for injury. Sports Med13. Taylor AJ, George KP. Ankle to brachial pressure index in1994; 17: 117-31normal subjects and trained cyclists with exercise induced leg

37. Davis RR, Hull ML. Measurement of pedal loading in bicycling:pain. Med Sci Sports Exerc 2001; 33 (11): 1862-7II. Analysis and results. J Biomech 1981; 14: 857-7214. Abraham P, Chevalier JM, Loire R, et al. External iliac artery

38. Coyle EF, Feltner ME, Kautz SA, et al. Physiological andendofibrosis in a young cyclist. Circulation 1999; 100: e38biomechanical factors associated with elite endurance cycling15. Rousselet MC, Saint Andre JP, L’Hoste PH, et al. Stenoticperformance. Med Sci Sports Exerc 1991; 23 (1): 93-107intimal thickening of the external iliac artery in competition

39. Fernandez-Garcia B, Alvarez J, Fernandez JA, et al. Diagnosingcyclists. Hum Pathol 1990; 21: 524-9external iliac artery endofibrosis by post-exercise ankle to arm16. Abraham P, Chevalier JM, Leftheriotis G, et al. Lower extremi-index in cyclists. Med Sci Sports Exerc 2002; 34 (2): 222-7ty disease in sports. Am J Sports Med 1997; 25 (4): 581-4

40. Abraham P, Bickert S, Chevalier JM, et al. Pressure measure-17. Abraham P, Saumet JL, Chevalier JM. External iliac arteryments at rest and after heavy exercise to detect moderateendofibrosis in athletes. Sports Med 1997; 24: 221-6arterial lesions in athletes. J Vasc Surg 2001 Apr; 33 (4): 721-718. Abraham P, Leftheriotis G, Bourre Y, et al. Echography of

external iliac artery endofibrosis in athletes. Am J Sports Med 41. Schwarzer AC, April CN, Bogduk N. The sacroiliac joint in1993; 21: 861-3 chronic low back pain. Spine 1995; 20: 31-7












https://www.researchgate.net/publication/14906938_Echography_of_external_iliac_artery_endofibrosis_in_cyclists?el=1_x_8&enrichId=rgreq-b7a52af6112ee8d19bb23bb24ace2a76-XXX&enrichSource=Y292ZXJQYWdlOzg0NzQzNDU7QVM6MTAyMTUzNjU4MDQ0NDM2QDE0MDEzNjY3Mzg3MDU=











is prohibited.

442 Bender et al.

42. Desvaux B, Abraham P, Colin D, et al. Ankle systolic blood 48. Wijesinghe LD, Coughlin PA, Robertson I, et al. Cyclists’s iliacpressure following submaximal and maximal exercise in syndrome: temporary relief by balloon angioplasty. Br J Sportsyoung men. J Sports Med Phys Fitness 1995; 35: 127-30 Med 2001; 35: 70-1

43. Desvaux B, Abraham P, Colin D, et al. Ankle to arm index 49. Hoes MJAJM, Binkhorst RA, Smeekes-Kuyl AEMC, et al.following maximal exercise in normal subjects and athletes. Measurement of forces on pedal and crank during work on aMed Sci Sport Exerc 1996; 28: 836-9 bicycle ergometer at different loads. Int Z Angew Physiol

44. Jager KA, Philips DJ, Martin RL. Non-invasive mapping of Einschl Arbeitsphysiol 1968; 26: 33-42lower limb arterial lesions. Ultrasound Med Biol 1985; 11: 50. Hull ML, Davis RR. Measurement of pedal loading in bicycling:515-21 I. Instrumentation. J Biomech 1981; 14: 843-56

45. Kohler TR, Nance DR, Cramer MM. Duplex scanning for51. Van Beekvelt MC, Colier WN, Wevers RA, et al. Performancediagnosis of aorto-iliac and femoropopliteal disease: a pro-

of near-infrared spectroscopy in measuring local O2 consump-spective study. Circulation 1987; 76: 1074-80tion and blood flow in skeletal muscle. J Appl Physiol 2001; 90

46. Strandness DE, Dawson DL. Indirect non-invasive testing and (2): 511-9duplex scanning. In: Strandness DE, van Breda A, editors.Vascular diseases, surgical and interventional therapy. NewYork: Churchill Livingstone, 1994: 139-99 Correspondence and offprints: Dr Goof Schep, Department

47. Fitzgibbon GM, Kafka HP, Leach AJ. Coronary bypass fate andof Sportsmedicine, Maxima Medical Centre, PO Box 7777,patient outcome: angiographic follow-up of 5065 grafts related5500 MB Veldhoven, The Netherlands.to survival and reoperation in 1388 patients during 25 years. J

Am Coll Cardiol 1996; 28: 616-26 E-mail: [email protected]


sports-related flow limitations in the iliac arteries in endurance athletes

Documents