SCHEP, GOOF; KAANDORP, DAVE W.; M. BENDER, MART H.; VAN ENGELAND, SASKIA; WEERDENBURG, HANS; TITULAER, BART M.; F. WIJN, PIETER F.
Pain, a feeling of powerlessness, and/or cramp in the legs when cycling over 40 km·h−1 may sound like a normal physiological response for most people. However, in high-level competitive cyclists, these complaints with typical claudication characteristics prove to be quite specific for flow limitations in the iliac arteries because approximately 60% of the athletes suffering from these complaints can be diagnosed as suffering from flow limitations in the iliac arteries (14,17). No clear epidemiological data are available. This is partly due to the fact that conventional diagnostic tests often fail in these patients, which leads to considerable under reporting of this diagnosis (1–3,6,17). Only recently was an accurate clinical decision algorithm to diagnose such flow limitations described, based upon sports-specific tests encompassing provocative exercise testing, echo-Doppler examination, and magnetic resonance angiography (MRA) (14,17). By using this protocol, 5 of 25 cyclists and triathletes who were members of the Dutch national team for the Olympic Games in 2000 had been diagnosed in the last few years as suffering from flow limitations and were successfully treated surgically (14). Although a formal epidemiological study is necessary to obtain reliable figures, a prevalence of 20% in such a selected group of Olympic athletes indicates that the number of endurance athletes with flow limitations in the iliac arteries must be substantial.
Intravascular narrowing due to endofibrosis (a reaction in the vessel wall due to mechanical loading) is commonly recognized as a cause for such flow limitations (1,2,6,7,12). However, kinking in the common iliac artery and/or external iliac artery may also be responsible (14,17,18). This kinking is caused by the repetitive hip flexion that occurs in cycling.
The anatomic location of the iliac arteries is ventral to the axis of movement of the hip joint on the psoas muscle. Therefore, when the hip flexes, it causes excessive length in these iliac arteries. Such excessive length can be accommodated for by the natural longitudinal elasticity of the vessel or by an increase in tortuosity of the vessels. If the iliac artery is fixed, for example, due to a side branch to the psoas muscle, a tethering of the artery with resultant kinking could occur during hip flexion (17). Apart from kinking due to tethering of the artery, extremely excessive lengths of the arteries are described in some of those patients (1,6,17). Also extreme vessel length leads to increased tortuosity and can therefore result in kinking.
The recommended treatment for flow limitations in the iliac arteries is conservative encompassing avoidance provocative sports like cycling and speed skating (1,3,17). When the athlete considers continuation of the provocative sports activity of paramount importance, kinking of the iliac arteries can be treated by surgical release of the iliac arteries (14,17). In this procedure, an inguinal incision about 4 cm wide is made parallel and 4 cm cranial of the inguinal ligament. The medial starting point of the incision is just lateral of the straight abdominal muscle. The abdominal muscles are split in line with the muscle fibers. The external iliac artery is located and a release of the underlying surface and the vascular sheath is performed in the caudo-cranial direction. If present, psoas branches are localized, clipped, and released. In particular, the iliac bifurcation often proves to be fixed to surrounding tissue, in contrast to findings observed during cadaver studies (8,10). When kinking occurs at the level of the common iliac artery (48% of cases (18)), it is necessary to mobilize the common iliac artery up to the aortic bifurcation. Great care must be taken not to damage the surrounding structures like the ureters, the iliac veins, and, when operating on the right side, the inferior vena cava. The use of an endoscopic videocamera enables safe meticulous dissection, and we observed no complications in the first 50 patients that were operated.
Postoperatively, to avoid unfavorable fixation by scar tissue, patients are instructed for the first 2 wk to repeatedly flex the hip passively and, for the first 6 wk, endurance exercise with intermittent hip flexion is restricted to walking and short cycling bouts at low intensity. Satisfactory results are described from this intervention including successful return to competition at the desired level in 20 of 23 (87%) endurance athletes suffering from flow limitation in the iliac arteries due to kinking of the iliac arteries (14). However, this surgical mobilization is only curative in selected patients in whom limited intravascular damage is encountered and in whom the kinking is not caused by excessive lengths of the arteries (14). If such intravascular narrowing and/or excessive vessel length is present, simple mobilization will not be effective and endarteriectomy or arterial reconstruction by a venous graft might be considered, entailing a considerably higher risk however (1,3,6,7,17). Percutaneous transluminal angioplasty and vascular stenting, although effective in iliac stenosis in atherosclerotic patients (4), prove not effective in the endofibrotic lesions encountered in these endurance athletes and have an increased risk for complications (5,13,15,16).
Because no normal values are available for vessel lengths in these endurance athletes, the current study is aimed at developing a scoring method for iliac artery vessel lengths with the hip extended and flexed in order to obtain normal values for this particular group of athletes. Such information will provide more objective information to assist decision making about whether surgical mobilization is possible or not.
Another aim of the study is to obtain further insight into the abnormalities encountered in endurance athletes with iliac artery flow limitations. Such knowledge of the normal and abnormal vessel movements will lead to a better understanding of the underlying mechanism for these flow limitations and consequently to improved determination of the most appropriate treatment.
In a prospective study from 1996 to 1999, 46 symptomatic legs in 42 patients suffering from flow limitations in the iliac arteries were examined with magnetic resonance angiography (MRA) with the hips flexed and extended. All patients met the following criteria: Active in endurance sports involving the legs (>5 h a week for more than 3 yr). Suffering from pain, feelings of powerlessness, and/or cramp in the leg at maximal effort, which disappears at rest. The complaints were not restricted to a localized area in a single muscle or tendon. A diagnosis of flow limitation in the iliac arteries was made after a validated clinical decision algorithm based mainly on the results of ankle pressure measurements after a provocative cycling test and echo-Doppler examination of the iliac arteries (14).
Sixteen healthy high-level competitive cyclists without complaints suggesting flow limitations served as a control group to obtain normal values. The general characteristics of both groups are shown in Table 1. The control group was well matched for sports activities with even a slightly higher working capacity, but they were slightly younger (Table 1).
The study was approved by the medical ethical committee of the Saint Joseph Hospital, Veldhoven, The Netherlands. All patients and control subjects gave informed written consent.
MRA was performed on a Philips Gyroscan NT 1.0T scanner (Philips Medical Systems, Best, The Netherlands). In all examinations, the distal aorta, common iliac artery, iliac bifurcation, external iliac artery, femoral artery, and femoral bifurcation were visualized. Detailed scan parameters are summarized in Table 2.
MRA with hips extended.
In the beginning of the study, an inflow scan was used as the imaging method with the hips extended. This inflow scan was available for all patients and members of the control group.
Inflow techniques, historically called “time of flight” techniques, consist of methods that use the motion of blood relative to surrounding tissue for the generation of contrast (9). The difference in saturation is not based on magnetic relaxation properties but purely on the differences in velocity. Inherently, this technique obtains hemodynamical information, i.e., the flow of blood, but presents this information in the form of a bright blood angiogram. A disadvantage of this technique is that it is very sensitive to movement, which results in artifacts in the images. This movement can be caused by the patient or by the vessel itself. Another disadvantage is the dependence on the direction of the flow, as it must be perpendicular to the transverse-imaging slice. Thus, tortuous vessels produce artifacts, because the blood becomes saturated when the artery runs in the transverse-imaging slice, which results in signal loss. Although in the iliac region the vessels normally run predominantly cranio-caudally, especially in some of our patients, there was increased tortuosity of the vessels, and the inflow technique proved less useful in such cases.
In 1997, a new scan technique was initiated using gadolinium-DTPA (diethylene triamine penta acetic acid) as a contrast agent (11). Its optimal scan volume is chosen based upon an inflow scan. A total of 30-mL gadolinium is evenly administered intravenously over 90 s, and the acquisition of the arterial phase is initiated about 20–30 s after the start of the injection.
Because the image contrast in gadolinium-enhanced angiography is strictly based on the presence of contrast agents in the blood irrespective of flow, this technique provides purely anatomical information. The advantage of this scan is that it inherently gives an anatomic representation of the vessel. This technique provides a better resolution and fewer artifacts (Table 2). In Figure 1, images obtained with both techniques are shown. It is evident that gadolinium enhancement improves the image quality. This is of considerable clinical importance, especially concerning the scoring of intravascular lesions. Vessel lengths, however, can be measured with the same reliability on images obtained by inflow techniques.
MRA with hips flexed.
Patients were positioned on their right side with the thighs flexed on the trunk and immobilized by the gantry of our scanner. Sagittal volumes were acquired before and during arterial bolus passage of gadolinium, and magnitude subtracted for background suppression. Gadolinium was administered according to the same scheme as in the scan with extended hips. Detailed scan parameters are listed in Table 2.
Postprocessing of the MRA data.
MRA can provide three-dimensional (3D) information about vessel lengths and the interrelationships of vessels with other structures (Fig. 2). To determine the degree of excessive length in the iliac arteries, both MRA examinations (hips extended and flexed) were used. The lengths of the arteries and possible kinkings were judged on images that were postprocessed with AnalyzeTM (CN Software Inc, Rochester, MN). The vessels were segmented, and maximum intensity projections were made (18). For determination of lengths of the vessel trajectories, four projections of the measuring volume were used. The vessel trajectories were followed by placing trace points in the center of the arteries in all four projections. The correct position of these points in the 3D-measurement volume was checked/verified on all four projections.
The first point of the common iliac artery was laid at the aortic bifurcation (Figs. 3 and 4). The common iliac artery was then traced further by selecting points along the artery until the bifurcation of the common iliac artery was reached (Figs. 3 and 4A and C). The external iliac artery was traced from the bifurcation of the common iliac artery to the bifurcation of the femoral artery (Fig. 4B and D). This procedure in AnalyzeTM generated four trace files that contained the trace points of both common iliac arteries and both external iliac arteries. With these points, the length of the arteries and the straight-line distance between the bifurcations were calculated.
The ratio between the length of an artery and the straight-line distance between the starting and the endpoint of the trace is used to measure the degree of excessive length in the arteries. The MRA examinations were all scored retrospectively by an investigator who was blinded to the subjects’ clinical diagnosis.
Differences in continuous variables were tested using Student’s t-test. Ranges are given as mean ± SD. For categorical variables, chi-square testing was used. The significance level was set at P < 0.05.
Left versus right leg in the reference group.
Both with the hips extended and flexed, vessel lengths, straight-line distances, and length ratios proved to be equal in the left and right legs in the reference group. Therefore, in all further analysis, the left and right reference legs were added together as one reference group of 32 reference legs. The length of the common iliac artery amounted to 7.4 ± 1.4 cm and 7.3 ± 1.6 cm with the hips extended and flexed, respectively. The lengths of the external iliac artery amounted to16.2 ± 2.0 cm and 14.3 ± 1.8 cm with the hips extended and flexed, respectively.
Symptomatic legs versus reference legs and asymptomatic legs.
In the common iliac artery, both with the hips extended and the hips flexed, the ratios of vessel length to straight-line distance were significantly higher in the symptomatic and asymptomatic legs compared with the reference legs (Table 3). In the external iliac artery, the ratios were significantly higher in the symptomatic and asymptomatic legs compared with the reference legs, in the flexed hip position only (Table 3). All length ratios exhibited a higher standard deviation in the symptomatic and asymptomatic legs than in the reference legs.
In Figure 5, a graphical representation of the observed ratios is given. It is demonstrated that the reference legs show a near normal distribution for all ratios. It is evident that in the patient group a subgroup of the symptomatic and asymptomatic legs has extremely high length ratios of their vessels, which explains the observed differences in standard deviations. Figures 6 and 7 show examples of a normal control and two patients with different length ratios of their vessels.
The current findings demonstrate that the ratio of vessel length to straight-line distance of the common iliac artery with the hip extended and of both the external and common iliac arteries with the hip flexed is significantly higher in patients suffering from flow limitations in the iliac arteries than in healthy reference endurance athletes. This is due to a subgroup of the patients in whom these length ratios are drastically increased.
The patients in this study were all endurance athletes with leg complaints diagnosed as due to flow limitations in the iliac arteries (3,6). The control subjects were a well-matched group of cyclists with even a higher exercise capacity than the patients. The average age of these control subjects was 8 yr younger. Because it is possible that vessel length increases with age, an analysis to the relation of age and vessel length proved mandatory. Therefore, a correlation analysis with age and all measured vessel lengths, straight-line distances, and length ratios was performed in both the patient group and the control group. There proved to be no significant correlation between age and any of the denominators of vessel length. It is therefore most unlikely that the age difference between patients and controls has had any significant modification in the observed differences between patients and reference persons.
Variations in height between individuals will influence vessel lengths and straight-line distances of vessel trajectories. By using length ratios, these variations will be accounted for, and different subjects can be compared. We therefore chose to do our main analysis on vessel length ratios only.
Figures 6 and 7 illustrate subjects with different length ratios and give an impression how the vessels with different length ratios appear, without performing the necessary calculations. The patient with a moderately excessive length suffered from claudication in his left leg mainly due to kinking in the common and external iliac arteries. This kinking in the common iliac artery is visible in Figure 7, although it is not viewed from the most appropriate projection (which would be with the kinking exactly in the plane of projection) (18). This patient could be treated successfully just with surgical release.
The patient with extremely excessive lengths suffered from claudication in the right leg more than in the left leg. The main cause for this claudication was a kinking in the external iliac artery, which is depicted in Figure 7. This patient was treated successfully with surgical release combined with a vascular reconstruction encompassing shortening of the external iliac artery.
The underlying causes for flow limitations in the iliac arteries can be intravascular lesions, kinking, or a combination of the two (1,3,6,14,17,18). The abnormalities can be located in the external iliac artery or in the common iliac artery or in both (1,3,6,14,17,18).
When surgical treatment of these flow limitations is considered, it is important to have exact information about the underlying cause. In a majority of patients, kinking proves to be the major underlying cause, and surgical treatment encompassing release of the common and external iliac arteries from psoas branches and adhesions will be successful (14). However, if kinking is caused by excessive vessel length, a simple release will not be curative, and a release combined with shortening of the vessels might be necessary (14). This latter operation carries a greater risk because it entails a vascular reconstruction.
The complaints of endurance athletes suffering from flow limitations in the iliac arteries are not life-threatening, and therefore careful consideration has to given to weighing the risks of treatment and the potential benefits. The risk of a vascular reconstruction outweighs the benefits in a large proportion of these patients. Iliac mobilization is an intervention with a considerably lower risk Therefore, in a larger proportion of patients the benefits of this intervention may outweigh the risks. However, excessive lengths of the arteries may interfere with the benefit that can be obtained from surgical release of the iliac arteries. Therefore, preoperative examination to define the vessel lengths, and compare these lengths to the maximum lengths, which still allow benefit from surgical release of the iliac arteries, is necessary.
In patients in whom a vascular reconstruction is considered worthwhile, it is important to have information not only of possible intravascular lesions but also of the exact excessive lengths of both the common and external iliac arteries to determine the most optimal surgical intervention. The best parameter to evaluate whether there is absolute excessive length consists of the ratio between the vessel length and the straight-line distance with the hips extended. The iliac arteries are ventral to the axis of movement of the hip joint and consequently, hip flexion produces excess length in the iliac arteries, which is why an absolute anatomic length excess can only be measured with the hips extended.
It is obvious that an increased length of the arteries leads to increased tortuosity thereby increasing the risk for kinking. The values in the reference legs with the hip extended as represented in Figure 5 can be considered to be healthy reference values. From Figure 5 it is clear that most patients do have vessel lengths in this normal range, while a minor subgroup of patients has vessel lengths far beyond this normal range. We therefore believe that for this latter subgroup of patients with length ratios for the common and external iliac artery above 1.15 and 1.25 respectively, a simple release of the iliac arteries may not be effective. Further prospective research is still necessary to determine the more precise border values of excessive lengths that are tolerated without complaints.
MRA has proven to be a valuable diagnostic instrument to visualize and measure the lengths of the common and external iliac arteries in endurance athletes with flow limitations, both with the hips extended and the hips flexed. The ratio between the vessel length and the straight-line distance for the common iliac artery and the external iliac artery with the hips flexed denominates excessive vessel length during hip flexion and proves to have the best discriminative property between symptomatic legs and reference legs.
The ratio between vessel length and the straight-line distance with the hips extended is the best parameter to judge whether there is an absolute excessive length. For the external iliac artery, a length ratio over 1.25, and for the common iliac artery, a ratio over 1.15 is abnormal. Further prospective study is needed in patients who will be treated surgically by mobilization of the iliac arteries to define maximal vessel lengths that still allow benefit from this operation.
This study was supported by grants from the Saint Joseph Hospital, Veldhoven, The Netherlands, the Dutch Olympic Committee/Dutch Sports Federation (NOC/NSF), and the Dutch Ministry of Health, Welfare and Sports (VWS), Department of Sports.
Address for correspondence: Goof Schep, Saint Joseph Hospital, Department of Sports Medicine, P.O. Box 7777, 5500MB Veldhoven, The Netherlands; E-mail: firstname.lastname@example.orgL.
1. Abraham, P., J. M. Chevalier, G. Leftheriotis, and J. L. Saumet. Lower extremity disease in sports. Am. J. Sports Med.
25:4, 581–584, 1997.
2. Abraham, P., G. Leftheriotis, Y. Bourre, J. M. Chevalier, and J. L. Saumet. Echography of external iliac artery endofibrosis in cyclists. Am. J. Sports Med.
21:6, 861–863, 1993.
3. Abraham, P., J. L. Saumet, and J. M. Chevalier. External iliac endofibrosis in athletes. Sportsmedicine 4: 221–226, 1997.
4. Bosch, J. L., and M. G. M. Hunink. Meta analysis of the results of percutaneous transluminal angioplasty and stent placement for aortoiliac occlusive disease. Radiology 204: 87–96, 1997.
5. Bradshaw, C. Exercise related lower leg pain: vascular. Med. Sci. Sports Exerc. S34–S36, 2000.
6. Chevalier, J. M. Vascular pathology of the cyclist. In:Encyclopedie Medico-Chirurgicale Francaise
A10, 11-675, 1997.
7. Chevalier, J. M., B. Enon, J. Walder, et al. Endofibrosis of the external iliac artery in bicycle racers: an unrecognized pathological state. Ann. Vasc. Surg. 1: 297–303, 1986.
8. Hayek, von H. The behavior of the arteries during joint movement [in German]. Z. Anat. Entwickl. Gesch.
9. Kouwenhoven, M., C. J. G. Bakker, M. J. Hartkamp, and W. P. Th. M. Mali. MR angiographic imaging. In: Vascular Diagnostics, P. Lanzer and J. Rösch (Eds.). Heidelberg: Springer-Verlag, 1994, pp. 375–401.
10. Lopez, J. F., J. L. Magne, and J. Champetier. The femoral artery and flexion of the hip joint. Surg. Radiol. Anat. 11: 245–81, 1989.
11. Niendorf, H. P., A. Alhassan, Th. Balzer, W. Clausz, and I. Cornelius I. Safety and risk of gadolinium-DTPA: extended clinical experience after more than 5,000,000 applications. Adv. MRI Contrast
12. Rousselet, M. C., J. P. Saint-Andre, Ph. L’Hoste, B. Enon, A. Megret, and J. M. Chevalier. Stenotic intimal thickening of the external iliac artery in competition cyclists. Hum. Pathol. 21: 524–9, 1990.
13. Ruurda, J. P., A. Rijbroek, E. G. J. Vermeulen, W. Wisselink, and J. A. Rauwerda. Arterial insufficiency in athletes due to “endofibrosis.” Ned. Tijdschr. Heelkd. 9: 124–126, 2000.
14. Schep, G. Functional vascular problems in the iliac arteries in endurance athletes: a new concept to explain flow limitations. Doctoral dissertation, University of Utrecht, Dept. of Physiology and Sports Medicine, ISBN 90–393–2601–0, February 2001, pp. 19–55.
15. Schep, G., and M. H. M. Bender. Comment on the article “Arterial insufficiency in athletes due to ‘endofibrosis’”. Ned. Tijdschr. Heelkd. 9: 127–128, 2000.
16. Schep, G., and M. H. M. Bender. Letter to the MSSE editor concerning exercise-related lower leg pain-vascular. Med. Sci. Sports Exerc. 32: 1970–1971, 2000.
17. Schep, G., M. H. M. Bender, D. Kaandorp, E. R. Hammacher, and W. R. de Vries. Flow limitations in the iliac arteries in endurance athletes: current knowledge and directions for the future. Int. J. Sportsmed. 20: 421–428, 1999.
18. Schep, G., D. W. Kaandorp, M. H. M. Bender, H. Weerdenburg, S. van Engeland, and P. F. F. Wijn. Magnetic resonance angiography used to detect kinking in the iliac arteries in endurance athletes with claudication. Physiol. Meas. 22: 475–487, 2001.