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External Iliac Endofibrosis in Endurance Athletes: A Novel Case in an Endurance Runner and a Review of the Literature
Eur J Vasc Endovasc Surg 26, 629–634 (2003) doi: 10.1016/j.ejvs.2003.08.003, available online at http://www.sciencedirect.com on
External Iliac Endofibrosis in Endurance Athletes: A Novel Case in an Endurance Runner and a Review of the Literature S. J. Ford,* A. Rehman and A. W. Bradbury University Department of Vascular Surgery, Heartlands Hospital, Birmingham, UK Background. There is increasing recognition that high-performance athletes can develop symptomatic arterial flow restriction in one or both (15%) legs due to kinking and/or endofibrosis of their iliac arteries. Methods. Case report and review based on a Medline search of the literature. Results. A 51-year-old female, 24-hour endurance runner presented with a six-month history of rapidly progressing intermittent claudication affecting her right thigh and calf in the absence of classical risk factors for atherosclerosis. On the basis of invasive and non-invasive investigations, a provisional diagnosis of endofibrosis was made and she was treated successfully with angioplasty. Conclusions. The epidemiology, optimal investigation and treatment of iliac endofibrosis in endurance athletes is poorly described. Each individual unit’s experience is likely to be very small. A European register of such cases would increase our understanding of the condition and improve patient outcomes. Key Words: Endofibrosis; Iliac; Endurance athlete.
Introduction
Epidemiology
There is increasing recognition that high-performance athletes, predominantly professional cyclists, can develop symptomatic arterial flow restriction in one or both (15%) legs due to kinking and/or endofibrosis of their (predominantly external) iliac arteries.1 – 7 A 51-year-old female, 24-hour endurance runner recently presented to our unit with a six-month history of rapidly progressing intermittent claudication affecting her right thigh and calf in the absence of classical risk factors for atherosclerosis (please see illustrative case report below). A provisional diagnosis of endofibrosis was made and she was treated successfully with angioplasty. In the course of investigating and treating this patient, it became clear that there is a lack of information about the aetiology, presentation, diagnosis, treatment and outcome of this condition. We, therefore, conducted a Medline search 1966 – 2002 using the search terms ‘intermittent claudication’, ‘endofibrosis’, ‘iliac arteries’, ‘physical endurance’, ‘endurance athletes’, ‘bicycling’, ‘fibromuscular dysplasia’. We felt the results of that review would be of interest to readers of the EJVES.
At the present time it is impossible to estimate the true prevalence of this condition. The literature mostly consists single case reports or small series comprising only a handful of patients, often gathered over many years. The largest experience is that of Chevalier and colleagues (Lyon, France) who have reported on over 200 patients undergoing surgery over a 10-year period.7 In that series, 56% of patients were under 30 years of age and more than 90% were cyclists (15% professional, 48% top amateur, 28% recreational). The remaining patients, who were significantly older than the cyclists, comprised tri-athletes (3%), cross-country skiers (0.5%) or runners (4.5%). Other sportsmen such as body-builders8 and rugby players9 may also be at risk. There appears to be a direct relationship between the frequency of the condition and the distance cycled with the average being around 150,000 km10,11 and some having covered up to 450,000 km.12
*Corresponding author. S. J. Ford, C/O Professor A. W. Bradbury, University Department of Vascular Surgery, Lincoln House (Research Institute), Birmingham Heartlands Hospital, Bordesley Green East, Birmingham B9 5SS, UK. 1078–5884/060629 + 06 $35.00/0 q 2003 Published by Elsevier Ltd.
Site of Disease The external iliac artery is most commonly affected (c. 90%), followed by the common iliac and common femoral arteries (c. 5 – 10% each). In c. 10% of patients more than one segment is affected, there
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may be a left-sided predominance and c. 15% of patients have bilateral symptoms, although the prevalence of occult contralateral asymptomatic disease (see case report) may be much higher.
Other mechanisms It is possible, although at the present time unknown, whether venous and/or neurological abnormalities also contribute to the symptom complex reported by affected athletes.
Aetiology The aetiology remains incompletely defined but appears to be related to one or more of the following. Repeated stretching The external iliac artery runs ventral to the axis of the hip joint and is stretched upon hip flexion. This maybe exacerbated by psoas muscle hypertrophy.7 The aerodynamic position adopted by cyclists leads to extreme hip flexion, which may explain the propensity of this particular group to develop the condition. External compression As well as pushing down, professional cyclists also pull up on the pedals. As a result, the hip flexors, particularly psoas, become markedly hypertrophied, and it has been suggested that this may compress the iliac arteries. It has also been suggested that the external iliac artery might become compressed as it passes under the inguinal ligament due to hypertrophy of the abdominal musculature (primarily the external oblique). High flow It has been suggested that the supra-physiological blood flows generated in the iliac arteries of highperformance athletes leads to endothelial dysfunction13 and injury that through, as yet unknown mechanisms, leads to endofibrosis. Kinking It has been suggested that branches originating from the external iliac artery and entering psoas lead to tethering of the artery, which in turn exacerbates kinking upon hip flexion.2 The other proposed tether point is where the circumflex iliac, epigastric and pudendal arteries leave the external iliac as it passes under the inguinal ligament.14 Eur J Vasc Endovasc Surg Vol 26, December 2003
Pathology As a result of the above and possibly other unknown mechanisms, arterial flow restriction can occur due to kinking alone, luminal narrowing alone, or both. With regard to luminal narrowing, this appears to be due to what has been termed ‘endofibrosis’, which is histologically distinct from atherosclerosis and fibromuscular hyperplasia. Specifically, the lesion is characterised by stenotic intimal thickening caused by a moderately cellular loose connective tissue containing variable amounts of elastin and collagen. The cellular infiltrate can be stained with antibodies to actin and myosin.15 In addition to intimal fibrosis, recent histological evaluation of five stenotic external iliac vessels resected from four competitive female cyclists demonstrated a degree of medial and adventitial response to such stress, prompting the authors to favour the term ‘external iliac arteriopathy’.16
Presentation In our case, the patient had noticed a gradual and unexplained deterioration in her performance over a couple of years and had abandoned competitive running. However, it was only when she developed severe and rapidly progressive leg pain on what she would consider minimal exercise (running a few miles!) that she sought medical advice. It is clear from reviewing the literature that only a minority of affected athletes complain of typical claudication-type symptoms. Rather, they present with an unexplained deterioration in performance, ‘weakness’, ‘lack of power, ‘swelling’, and a ‘feeling of paralysis’.5 Whether these atypical symptoms represent true arterial (and venous?) (compression, kinking) or neurological (compression, stretching, ischaemia) is uncertain. However, as the symptoms usually vague and non-specific, findings on physical examination at rest often unremarkable, and the ‘super-fit’ are considered unlikely to develop vascular disease, there is often a long delay between symptoms first developing and the diagnosis being made (please see below).5,17 The average delay appears to be around
External Iliac Endofibrosis in Endurance Athletes
2 years (40,000 km cycling)7 during which time the athlete may be forced to drop out of competition, never to return.
Diagnosis In our case, the diagnosis was relatively straightforward as the patient presented late with symptoms typical of claudication and a reduced femoral pulse on the affected side on clinical examination. However, making a diagnosis at an earlier stage where the only ‘symptom’ is a non-specific impairment in performance and clinical examination is within normal limits may be much more problematic. Physical examination. The great majority of affected athletes will have normal pulses because the degree of luminal narrowing is insufficient to cause a clinically detectable pressure drop at rest, or because the underlying pathology is kinking that only manifests itself at the extremes of flexion. There may be a bruit but usually only after exercise and/or during maximum hip flexion.7 Ankle:Brachial Pressure Index (ABPI). Similarly, the ABPI will usually be normal at rest.10,18 Exercise may produce a detectable fall in ABPI but on cessation of exercise the pressure may return to normal so quickly that it is easily missed unless the ankle pressure is measured almost immediately. Furthermore, the normal practice of obtaining pressures with the patient supine and the hip extended may be inappropriate in such cases. Exercise testing. Apart from the rapid recovery in ABPI noted above, standard exercise testing is often uninformative because the exercise used is simply not extreme or prolonged enough to mimic the situation found during competition. Furthermore, treadmill testing may not mimic the muscle usage and extremes of hip flexion experienced by the athlete who are most often cyclists. Several groups have described specific cycle-ergometer based testing protocols designed to overcome these difficulties but clearly they are not widely available.5,7,10 Ultrasound examination. Even in expert hands the diagnosis can be difficult to make on ultrasound examination because velocities and waveforms are usually normal except at extremes of exercise and/or hip movement during which the artery is difficult to insonate. The only clue to the underlying pathophysiology may be an impression of mildly hyperechoic segmental myointimal thickening (c. 0.3 mm) in axial view, which is easily overlooked.10,18,19 Intra-vascular ultrasound (IVUS) can also show the degree and distribution of intimal thickening and may be a useful
631
adjunct when other investigations including angiography and measurement of pressure gradient (see below) are uninformative.20 Intra-arterial digital subtraction angiography (IADSA). Unless angiographic images are obtained in multiple planes and in different positions of hip flexion and extension, the subtle, irregular and eccentric angiographic abnormalities associated with the disease may be missed. The most characteristic angiographic finding appears to be a beaded or smooth stenotic appearance that most commonly starts just distal to the common iliac bifurcation and extends some 5– 6 cm down the external iliac artery.7,10 Calcification is typically absent. In some cases, narrowing of the arterial lumen can only be appreciated by directly comparing like images of the affected with the non-affected side. Pressure measurements are likely to be normal at rest but a gradient may become detectable across the affected segment after vasodilator induced distal vasodilatation.10 Magnetic resonance angiography (MRA). As yet, there is limited experience with Gadolinium enhanced MRA in this condition but the technique may represent a major advance7 as it is non-invasive, non-toxic, provides a resolution similar to IA-DSA, and images can be obtained in different hip positions and processed to provide 3-D reconstructions. This may aid diagnosis, provide further understanding with respect to aetiology and by differentiating kinking from luminal narrowing help to guide treatment. A prospective study,12 found MRA to be more sensitive than IA-DSA.
Treatment Once the diagnosis has been made, there is little consensus on optimal treatment and almost no data on the long-term outcomes. Best medical therapy (BMT). Although it intuitively makes sense to institute ‘best medical therapy’ (comprising smoking cessation, anti-platelet agents, statin therapy etc.), it must be remembered that ‘endofibrosis’ is distinct from atherosclerosis and the prevalence of conventional vascular risk factors is likely to be very low in this population. One report suggested a high prevalence of hyperhomocysteinaemia in affected individuals but the significance of this is, as yet, unknown.7 It has been suggested that the condition may improve over time with conservative therapy, and certainly progression to disabling claudication on walking or critical limb ischaemia seems very unlikely. In some cases it may be possible to modify the athletes level and type of activity to Eur J Vasc Endovasc Surg Vol 26, December 2003
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S. J. Ford et al.
ameliorate the symptoms. For example, cyclists can be advised to alter their riding position to reduce hip flexion and not to pull actively on the pedal. However, in many cases, without intervention the condition effectively spells the end of the athlete’s competitive career. Most authorities seem agreed that intervention should not be undertaken lightly and is only indicated once it is clear that all non-interventional options have been exhausted. The balance of risks and benefits is clearly going to be quite different for the recreational athlete and the Olympian. Endovascular therapy. Minimally invasive therapy has obvious attractions and previous authors have reported successful return to competition following percutaneous transluminal balloon angioplasty (PTBA).10 However, several authors have counselled against the use the use of PTBA for fear risk of initiating a dissection due to the loose attachment between the intimal endofibrotic lesion and the media at the internal elastic lamina.21,22 Concerns have also been expressed about the durability of angioplasty. There is a perception that histological nature of the lesion makes early elastic recoil and symptomatic recurrence likely,10 although in the case described here the patient remains symptomatically better 12 months after an uncomplicated angioplasty. Furthermore, symptomatic and haemodynamic improvement has been reported despite little increase in luminal diameter on the immediate post-angioplasty image.10 Repeated angioplasty is a theoretical option for symptomatic recurrence but there are no reports in the literature on which to base current practice. There are no reports of stenting in the literature but on first principles it would seem unwise for fear of mechanical compression and/or disintegration, and aggressive neo-intimal hyperplasia at the stent margins, due to the excessive movement. Surgery. There is a natural reluctance to subject these athletes to surgery because of the recuperation period, the risk of complications and concern about subjecting vascular anastomoses to such extreme repetitive strain. Several different procedures, either singly or in combination, have been advocated. In this respect, the crucial determinant seems to be distinguishing those patients in whom kinking is the underlying problem from those in whom there is either or also a haemodynamically significant luminal narrowing. There are several procedures described in the literature. 1. Arterial release. This involves dividing arterial branches, fascia and scar tissue tethering the iliac arteries to the psoas muscle and possibly at the inguinal ligament. This is only indicated when the Eur J Vasc Endovasc Surg Vol 26, December 2003
underlying problem is kinking and luminal narrowing has been confidently excluded.7 As the integrity of the artery is not breached the risks are likely to be minimal Shep and colleagues12 have described their operative technique and results in a prospective study of 23 patients (mean [range] age 30 [22 – 48] years, 21 men, 21 left leg). There were no complications and the mean hospital stay was only 3 days. Post-operatively, the patients underwent specific physiotherapy and a controlled re-introduction to their sport to reduce the risks of refibrosis. At a median (range) follow-up of six (4 – 36) months, all the patients improved subjectively, 12 were rendered asymptomatic and there was a significant improvement in ABPI and peak systolic velocities on Doppler examination. 2. Shortening of the artery. This is only appropriate if the underlying problem is kinking and there is clear arterial redundancy. This procedure obviously entails breaching the integrity of the artery. The length of artery that should be resected remains purely empirical and a matter of judgment on a case-by-case basis. 3. Resection of the fibrotic segment followed by saphenous vein interposition graft. This is indicated where there is narrowing but no arterial redundancy. As the saphenous vein is usually of lesser calibre than the artery to be replaced, and it is important not to replace one form of functional obstruction with another, panel and spiral grafts appear to be frequently required and advocated. There is general agreement that prosthetic graft materials should be avoided. 4. Endarterectomy and vein patch angioplasty.
Illustrative Case Report To our knowledge this is the first report associated with endurance running. The aim of this sport is to determine who can cover the furthest distance in 24 h; distances exceeding 100 km are apparently not uncommon. This case exemplifies many of the difficulties associated with this uncommon condition. A 51-year-old female, 24-hour endurance runner presented with a six-month history of rapidly progressing intermittent claudication affecting her right thigh and calf. As a result, her weekly training distance had reduced from over one hundred to only a few miles and she had abandoned competitive running. She was an ex-smoker of 20 years but has never smoked heavily. There were no other major vascular risk factors for arterial disease and no family history of
External Iliac Endofibrosis in Endurance Athletes
Fig. 1. Intra-arterial digital subtraction angiography of the right iliac vessels demonstrating an isolated short 5 cm proximal external iliac artery occlusion compatible with endofibrosis.
arterial disease. Her cholesterol level was 5.0 mmol/L and triglycerides 0.8 mmols/L. On physical examination, the left leg appeared normal but on the right the femoral and distal pulses were reduced. The resting ABPI was 0.89 on the left and 0.63 on the right. Intra-arterial digital subtraction angiography (IA-DSA) of the right leg demonstrated an isolated short 5 cm proximal external iliac artery occlusion compatible with endofibrosis (Figs. 1 and 2). The remaining vessels were normal bilaterally. The lesion was successfully treated with PTBA (Fig. 2). One year following the procedure the patient
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remains symptoms free with a normal right femoral pulse and has returned to competitive running. Although our patient appears to have had a good outcome, at least in the short term, the case does highlight a number of issues with regard to the investigation and treatment of this unusual condition and several questions remains unanswered. Was the diagnosis truly ‘endofibrosis’? The only vascular risk factor was very light smoking in early adulthood but without resecting the artery it is impossible to know whether this was endofibrosis, or atherosclerosis, or both. Why was the ABPI reduced on the left (the asymptomatic side)? Angiography appeared be normal but it is possible that further images in different planes may have revealed some disease. How durable will the angioplasty be? And, if the patient represents, would repeat angioplasty or surgery or no intervention be appropriate? Is there a role for ‘best medical therapy’ (statin, clopidogrel, cilostazol) in such patients?23 Is there a role for thrombophilia screening including measurement of homocysteine?24
Conclusions This is an uncommon condition and individual experience is likely to be small. Many questions remain unanswered with regard to prevalence, aetiology, diagnosis, treatment and prognosis. In common with many rare conditions, probably the best way of gaining and disseminating knowledge in the first instance is through a registry of cases. Any reader interested in developing and/or contributing to such a registry is encouraged to contact the senior author ([email protected]). Alternatively, if such a registry already exists, we would be pleased to contribute to it.
References
Fig. 2. Intra-arterial digital subtraction angiography of the right iliac vessels after successful percutaneous transluminal balloon angioplasty of the external iliac occlusion.
1 Mosimann R, Walder J, van Melle G. Stenotic intimal thickening of the external iliac artery: illness of the competition cyclists? J Vasc Surg 1985; 19: 258–263. 2 Chevalier JM, Enon B, Waider J, Barral X, Pillet J, Megret A, L’Hoste Ph, Saint-Adre JP, Davinroy M. Endofibrosis of the external iliac artery in bicycle racers: an unrecognised pathological state. Ann Vasc Surg 1986; 1: 297– 303. 3 Pils K, Bochdansky Th, Jantsch HS, Ernst E. Intermittent leg ischaemia during competition cycling. Lancet 1990; 336(8708): 189. 4 Scheerlinck TAM, van den Brande P. Post-traumatic iliac dissection and thrombosis of the external iliac artery in a youngman. Eur J Vasc Surg 1994; 8: 645 –647. 5 Abraham P, Chevalier JM, Saumet JL. External iliac artery Eur J Vasc Endovasc Surg Vol 26, December 2003
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6 7 8 9 10 11 12
13
14 15
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endofibrosis: a 40-year course. J Sports Med Phys Fitness 1997; 37: 297–300. Taylor AJ, Tennant WG, Batt ME, Wallace WA. Traumatic occlusion of the external iliac artery in a racing cyclist: a cause of ill-defined leg pain. Br J Sports Med 1997; 31: 155–156. Schep G, Bender M et al. Flow limitations in the iliac arteries in endurance athletes—current knowledge and directions for the future. Int J Sports Med 1999; 20: 421–428. Khaira HS, Awad RW, Aluwihare N et al. External iliac artery stenosis in a young body builder. Eur J Vasc Endovasc Surg 1996; 11: 499–501. Bray AE, Lewis WA. Intermittent claudication in a professional rugby player. J Vasc Surg 1992; 15: 664– 668. Wijesinghe LD, Coughlin PA, Robertson I, Kessel D, Kent PJ, Kester RC. Cyclist’s iliac syndrome: temporary relief by balloon angioplasty. Br J Sports Med 2001; 35: 70 –71. Abraham P, Saumet JL, Chevalier JM. External iliac endofibrosis in athletes. Sports Med 1997; 24: 221–226. Schep G, Bender MHM, van de Tempel G, Wijn PFF, de Vries WR, Eikelboom BC. Detection and treatment of claudication due to functional iliac obstruction in top endurance athletes: a prospective study. Lancet 2002; 359: 466. February. Wright IA, Pugh ND, Goodfellow J et al. Dynamic obstruction of the external iliac artery in endurance athletes and its relationship to endothelial function: the case of a long distance runner. Br J Sports Med 1997; 31: 156–158. Lopez J-F, Magne J-L, Champetier J. The femoral artery and flexion of the hip joint. Surg Radiol Anat 1989; 11: 275–283. Rousselet MC, Saint Andre JP, L’Hoste PH, Enon B, Megret A, Chevalier JM. Stenotic intimal thickening of the external iliac artery in competitive cyclists. Hum Pathol 1990; 21: 524–529.
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16 Kral CA, Han DC, Edwards WD, Spittell PC, Tazelaar HD, Cherry Jr. KJ. Obstructive external iliac arteriopathy in avid bicyclists: new and variable histopathological features in four women. J Vasc Surg 2002; 36(3): 565–570. Sep. 17 Sise MJ, Shackford SR, Rowley WR, Pistone FJ. Claudication in young adults: a frequently delayed diagnosis. J Vasc Surg 1989; 10(1): 68– 74. Jul. 18 Abraham P, Chevalier JM, Loire R, Saumet JL. External iliac endofibrosis in a young cyclist. Circulation 1999; 100: e38. 19 Abraham P, Leftheriotis G, Bourre Y, Chevalier JM, Saumet JL. Echography of external artery endofibrosis in cyclists. Am J Sportsmed 1993; 21: 861– 863. 20 Lomis NNT, Miller FJ, Whiting JH, Giuliano AW, Yoon H-C. Exercise-induced external iliac artery intimal fibrosis: confirmation with intravascular ultrasound. JVIR 2000; 11: 51 –53. 21 Cook PS, Erodes LS, Selzer PM, Rivera FJ, Palmaz JC. Dissection of external iliac artery in highly trained athletes. J Vasc Surg 1995; 22: 173–177. 22 Gallo D, Soury P, Pilsonnier D, Panet M, Peillon C, Testarts J, Watelet J. Aneurism Dissecant de l’arterie iliaque externe, une evolution inhabituelle de l’endofibrosie du sportif. J Mal Vasc 1996; 21: 95 –97. 23 Burns P, Gough S, Bradbury AW. Management of peripheral arterial disease in primary care. Br Med J 2003; 326(7389): 584 –588. 24 Bradbury AW, MacKenzie RK, Burns P, Fegan C. Thrombophilia and chronic venous ulceration. Eur J Vasc Endovasc Surg 2002; 24(2): 97–104. Accepted 11 August 2003
External Iliac Endofibrosis in Endurance Athletes: A Novel Case in an Endurance Runner and a Review of the Literature S. J. Ford,* A. Rehman and A. W. Bradbury University Department of Vascular Surgery, Heartlands Hospital, Birmingham, UK Background. There is increasing recognition that high-performance athletes can develop symptomatic arterial flow restriction in one or both (15%) legs due to kinking and/or endofibrosis of their iliac arteries. Methods. Case report and review based on a Medline search of the literature. Results. A 51-year-old female, 24-hour endurance runner presented with a six-month history of rapidly progressing intermittent claudication affecting her right thigh and calf in the absence of classical risk factors for atherosclerosis. On the basis of invasive and non-invasive investigations, a provisional diagnosis of endofibrosis was made and she was treated successfully with angioplasty. Conclusions. The epidemiology, optimal investigation and treatment of iliac endofibrosis in endurance athletes is poorly described. Each individual unit’s experience is likely to be very small. A European register of such cases would increase our understanding of the condition and improve patient outcomes. Key Words: Endofibrosis; Iliac; Endurance athlete.
Introduction
Epidemiology
There is increasing recognition that high-performance athletes, predominantly professional cyclists, can develop symptomatic arterial flow restriction in one or both (15%) legs due to kinking and/or endofibrosis of their (predominantly external) iliac arteries.1 – 7 A 51-year-old female, 24-hour endurance runner recently presented to our unit with a six-month history of rapidly progressing intermittent claudication affecting her right thigh and calf in the absence of classical risk factors for atherosclerosis (please see illustrative case report below). A provisional diagnosis of endofibrosis was made and she was treated successfully with angioplasty. In the course of investigating and treating this patient, it became clear that there is a lack of information about the aetiology, presentation, diagnosis, treatment and outcome of this condition. We, therefore, conducted a Medline search 1966 – 2002 using the search terms ‘intermittent claudication’, ‘endofibrosis’, ‘iliac arteries’, ‘physical endurance’, ‘endurance athletes’, ‘bicycling’, ‘fibromuscular dysplasia’. We felt the results of that review would be of interest to readers of the EJVES.
At the present time it is impossible to estimate the true prevalence of this condition. The literature mostly consists single case reports or small series comprising only a handful of patients, often gathered over many years. The largest experience is that of Chevalier and colleagues (Lyon, France) who have reported on over 200 patients undergoing surgery over a 10-year period.7 In that series, 56% of patients were under 30 years of age and more than 90% were cyclists (15% professional, 48% top amateur, 28% recreational). The remaining patients, who were significantly older than the cyclists, comprised tri-athletes (3%), cross-country skiers (0.5%) or runners (4.5%). Other sportsmen such as body-builders8 and rugby players9 may also be at risk. There appears to be a direct relationship between the frequency of the condition and the distance cycled with the average being around 150,000 km10,11 and some having covered up to 450,000 km.12
*Corresponding author. S. J. Ford, C/O Professor A. W. Bradbury, University Department of Vascular Surgery, Lincoln House (Research Institute), Birmingham Heartlands Hospital, Bordesley Green East, Birmingham B9 5SS, UK. 1078–5884/060629 + 06 $35.00/0 q 2003 Published by Elsevier Ltd.
Site of Disease The external iliac artery is most commonly affected (c. 90%), followed by the common iliac and common femoral arteries (c. 5 – 10% each). In c. 10% of patients more than one segment is affected, there
S. J. Ford et al.
630
may be a left-sided predominance and c. 15% of patients have bilateral symptoms, although the prevalence of occult contralateral asymptomatic disease (see case report) may be much higher.
Other mechanisms It is possible, although at the present time unknown, whether venous and/or neurological abnormalities also contribute to the symptom complex reported by affected athletes.
Aetiology The aetiology remains incompletely defined but appears to be related to one or more of the following. Repeated stretching The external iliac artery runs ventral to the axis of the hip joint and is stretched upon hip flexion. This maybe exacerbated by psoas muscle hypertrophy.7 The aerodynamic position adopted by cyclists leads to extreme hip flexion, which may explain the propensity of this particular group to develop the condition. External compression As well as pushing down, professional cyclists also pull up on the pedals. As a result, the hip flexors, particularly psoas, become markedly hypertrophied, and it has been suggested that this may compress the iliac arteries. It has also been suggested that the external iliac artery might become compressed as it passes under the inguinal ligament due to hypertrophy of the abdominal musculature (primarily the external oblique). High flow It has been suggested that the supra-physiological blood flows generated in the iliac arteries of highperformance athletes leads to endothelial dysfunction13 and injury that through, as yet unknown mechanisms, leads to endofibrosis. Kinking It has been suggested that branches originating from the external iliac artery and entering psoas lead to tethering of the artery, which in turn exacerbates kinking upon hip flexion.2 The other proposed tether point is where the circumflex iliac, epigastric and pudendal arteries leave the external iliac as it passes under the inguinal ligament.14 Eur J Vasc Endovasc Surg Vol 26, December 2003
Pathology As a result of the above and possibly other unknown mechanisms, arterial flow restriction can occur due to kinking alone, luminal narrowing alone, or both. With regard to luminal narrowing, this appears to be due to what has been termed ‘endofibrosis’, which is histologically distinct from atherosclerosis and fibromuscular hyperplasia. Specifically, the lesion is characterised by stenotic intimal thickening caused by a moderately cellular loose connective tissue containing variable amounts of elastin and collagen. The cellular infiltrate can be stained with antibodies to actin and myosin.15 In addition to intimal fibrosis, recent histological evaluation of five stenotic external iliac vessels resected from four competitive female cyclists demonstrated a degree of medial and adventitial response to such stress, prompting the authors to favour the term ‘external iliac arteriopathy’.16
Presentation In our case, the patient had noticed a gradual and unexplained deterioration in her performance over a couple of years and had abandoned competitive running. However, it was only when she developed severe and rapidly progressive leg pain on what she would consider minimal exercise (running a few miles!) that she sought medical advice. It is clear from reviewing the literature that only a minority of affected athletes complain of typical claudication-type symptoms. Rather, they present with an unexplained deterioration in performance, ‘weakness’, ‘lack of power, ‘swelling’, and a ‘feeling of paralysis’.5 Whether these atypical symptoms represent true arterial (and venous?) (compression, kinking) or neurological (compression, stretching, ischaemia) is uncertain. However, as the symptoms usually vague and non-specific, findings on physical examination at rest often unremarkable, and the ‘super-fit’ are considered unlikely to develop vascular disease, there is often a long delay between symptoms first developing and the diagnosis being made (please see below).5,17 The average delay appears to be around
External Iliac Endofibrosis in Endurance Athletes
2 years (40,000 km cycling)7 during which time the athlete may be forced to drop out of competition, never to return.
Diagnosis In our case, the diagnosis was relatively straightforward as the patient presented late with symptoms typical of claudication and a reduced femoral pulse on the affected side on clinical examination. However, making a diagnosis at an earlier stage where the only ‘symptom’ is a non-specific impairment in performance and clinical examination is within normal limits may be much more problematic. Physical examination. The great majority of affected athletes will have normal pulses because the degree of luminal narrowing is insufficient to cause a clinically detectable pressure drop at rest, or because the underlying pathology is kinking that only manifests itself at the extremes of flexion. There may be a bruit but usually only after exercise and/or during maximum hip flexion.7 Ankle:Brachial Pressure Index (ABPI). Similarly, the ABPI will usually be normal at rest.10,18 Exercise may produce a detectable fall in ABPI but on cessation of exercise the pressure may return to normal so quickly that it is easily missed unless the ankle pressure is measured almost immediately. Furthermore, the normal practice of obtaining pressures with the patient supine and the hip extended may be inappropriate in such cases. Exercise testing. Apart from the rapid recovery in ABPI noted above, standard exercise testing is often uninformative because the exercise used is simply not extreme or prolonged enough to mimic the situation found during competition. Furthermore, treadmill testing may not mimic the muscle usage and extremes of hip flexion experienced by the athlete who are most often cyclists. Several groups have described specific cycle-ergometer based testing protocols designed to overcome these difficulties but clearly they are not widely available.5,7,10 Ultrasound examination. Even in expert hands the diagnosis can be difficult to make on ultrasound examination because velocities and waveforms are usually normal except at extremes of exercise and/or hip movement during which the artery is difficult to insonate. The only clue to the underlying pathophysiology may be an impression of mildly hyperechoic segmental myointimal thickening (c. 0.3 mm) in axial view, which is easily overlooked.10,18,19 Intra-vascular ultrasound (IVUS) can also show the degree and distribution of intimal thickening and may be a useful
631
adjunct when other investigations including angiography and measurement of pressure gradient (see below) are uninformative.20 Intra-arterial digital subtraction angiography (IADSA). Unless angiographic images are obtained in multiple planes and in different positions of hip flexion and extension, the subtle, irregular and eccentric angiographic abnormalities associated with the disease may be missed. The most characteristic angiographic finding appears to be a beaded or smooth stenotic appearance that most commonly starts just distal to the common iliac bifurcation and extends some 5– 6 cm down the external iliac artery.7,10 Calcification is typically absent. In some cases, narrowing of the arterial lumen can only be appreciated by directly comparing like images of the affected with the non-affected side. Pressure measurements are likely to be normal at rest but a gradient may become detectable across the affected segment after vasodilator induced distal vasodilatation.10 Magnetic resonance angiography (MRA). As yet, there is limited experience with Gadolinium enhanced MRA in this condition but the technique may represent a major advance7 as it is non-invasive, non-toxic, provides a resolution similar to IA-DSA, and images can be obtained in different hip positions and processed to provide 3-D reconstructions. This may aid diagnosis, provide further understanding with respect to aetiology and by differentiating kinking from luminal narrowing help to guide treatment. A prospective study,12 found MRA to be more sensitive than IA-DSA.
Treatment Once the diagnosis has been made, there is little consensus on optimal treatment and almost no data on the long-term outcomes. Best medical therapy (BMT). Although it intuitively makes sense to institute ‘best medical therapy’ (comprising smoking cessation, anti-platelet agents, statin therapy etc.), it must be remembered that ‘endofibrosis’ is distinct from atherosclerosis and the prevalence of conventional vascular risk factors is likely to be very low in this population. One report suggested a high prevalence of hyperhomocysteinaemia in affected individuals but the significance of this is, as yet, unknown.7 It has been suggested that the condition may improve over time with conservative therapy, and certainly progression to disabling claudication on walking or critical limb ischaemia seems very unlikely. In some cases it may be possible to modify the athletes level and type of activity to Eur J Vasc Endovasc Surg Vol 26, December 2003
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ameliorate the symptoms. For example, cyclists can be advised to alter their riding position to reduce hip flexion and not to pull actively on the pedal. However, in many cases, without intervention the condition effectively spells the end of the athlete’s competitive career. Most authorities seem agreed that intervention should not be undertaken lightly and is only indicated once it is clear that all non-interventional options have been exhausted. The balance of risks and benefits is clearly going to be quite different for the recreational athlete and the Olympian. Endovascular therapy. Minimally invasive therapy has obvious attractions and previous authors have reported successful return to competition following percutaneous transluminal balloon angioplasty (PTBA).10 However, several authors have counselled against the use the use of PTBA for fear risk of initiating a dissection due to the loose attachment between the intimal endofibrotic lesion and the media at the internal elastic lamina.21,22 Concerns have also been expressed about the durability of angioplasty. There is a perception that histological nature of the lesion makes early elastic recoil and symptomatic recurrence likely,10 although in the case described here the patient remains symptomatically better 12 months after an uncomplicated angioplasty. Furthermore, symptomatic and haemodynamic improvement has been reported despite little increase in luminal diameter on the immediate post-angioplasty image.10 Repeated angioplasty is a theoretical option for symptomatic recurrence but there are no reports in the literature on which to base current practice. There are no reports of stenting in the literature but on first principles it would seem unwise for fear of mechanical compression and/or disintegration, and aggressive neo-intimal hyperplasia at the stent margins, due to the excessive movement. Surgery. There is a natural reluctance to subject these athletes to surgery because of the recuperation period, the risk of complications and concern about subjecting vascular anastomoses to such extreme repetitive strain. Several different procedures, either singly or in combination, have been advocated. In this respect, the crucial determinant seems to be distinguishing those patients in whom kinking is the underlying problem from those in whom there is either or also a haemodynamically significant luminal narrowing. There are several procedures described in the literature. 1. Arterial release. This involves dividing arterial branches, fascia and scar tissue tethering the iliac arteries to the psoas muscle and possibly at the inguinal ligament. This is only indicated when the Eur J Vasc Endovasc Surg Vol 26, December 2003
underlying problem is kinking and luminal narrowing has been confidently excluded.7 As the integrity of the artery is not breached the risks are likely to be minimal Shep and colleagues12 have described their operative technique and results in a prospective study of 23 patients (mean [range] age 30 [22 – 48] years, 21 men, 21 left leg). There were no complications and the mean hospital stay was only 3 days. Post-operatively, the patients underwent specific physiotherapy and a controlled re-introduction to their sport to reduce the risks of refibrosis. At a median (range) follow-up of six (4 – 36) months, all the patients improved subjectively, 12 were rendered asymptomatic and there was a significant improvement in ABPI and peak systolic velocities on Doppler examination. 2. Shortening of the artery. This is only appropriate if the underlying problem is kinking and there is clear arterial redundancy. This procedure obviously entails breaching the integrity of the artery. The length of artery that should be resected remains purely empirical and a matter of judgment on a case-by-case basis. 3. Resection of the fibrotic segment followed by saphenous vein interposition graft. This is indicated where there is narrowing but no arterial redundancy. As the saphenous vein is usually of lesser calibre than the artery to be replaced, and it is important not to replace one form of functional obstruction with another, panel and spiral grafts appear to be frequently required and advocated. There is general agreement that prosthetic graft materials should be avoided. 4. Endarterectomy and vein patch angioplasty.
Illustrative Case Report To our knowledge this is the first report associated with endurance running. The aim of this sport is to determine who can cover the furthest distance in 24 h; distances exceeding 100 km are apparently not uncommon. This case exemplifies many of the difficulties associated with this uncommon condition. A 51-year-old female, 24-hour endurance runner presented with a six-month history of rapidly progressing intermittent claudication affecting her right thigh and calf. As a result, her weekly training distance had reduced from over one hundred to only a few miles and she had abandoned competitive running. She was an ex-smoker of 20 years but has never smoked heavily. There were no other major vascular risk factors for arterial disease and no family history of
External Iliac Endofibrosis in Endurance Athletes
Fig. 1. Intra-arterial digital subtraction angiography of the right iliac vessels demonstrating an isolated short 5 cm proximal external iliac artery occlusion compatible with endofibrosis.
arterial disease. Her cholesterol level was 5.0 mmol/L and triglycerides 0.8 mmols/L. On physical examination, the left leg appeared normal but on the right the femoral and distal pulses were reduced. The resting ABPI was 0.89 on the left and 0.63 on the right. Intra-arterial digital subtraction angiography (IA-DSA) of the right leg demonstrated an isolated short 5 cm proximal external iliac artery occlusion compatible with endofibrosis (Figs. 1 and 2). The remaining vessels were normal bilaterally. The lesion was successfully treated with PTBA (Fig. 2). One year following the procedure the patient
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remains symptoms free with a normal right femoral pulse and has returned to competitive running. Although our patient appears to have had a good outcome, at least in the short term, the case does highlight a number of issues with regard to the investigation and treatment of this unusual condition and several questions remains unanswered. Was the diagnosis truly ‘endofibrosis’? The only vascular risk factor was very light smoking in early adulthood but without resecting the artery it is impossible to know whether this was endofibrosis, or atherosclerosis, or both. Why was the ABPI reduced on the left (the asymptomatic side)? Angiography appeared be normal but it is possible that further images in different planes may have revealed some disease. How durable will the angioplasty be? And, if the patient represents, would repeat angioplasty or surgery or no intervention be appropriate? Is there a role for ‘best medical therapy’ (statin, clopidogrel, cilostazol) in such patients?23 Is there a role for thrombophilia screening including measurement of homocysteine?24
Conclusions This is an uncommon condition and individual experience is likely to be small. Many questions remain unanswered with regard to prevalence, aetiology, diagnosis, treatment and prognosis. In common with many rare conditions, probably the best way of gaining and disseminating knowledge in the first instance is through a registry of cases. Any reader interested in developing and/or contributing to such a registry is encouraged to contact the senior author ([email protected]). Alternatively, if such a registry already exists, we would be pleased to contribute to it.
References
Fig. 2. Intra-arterial digital subtraction angiography of the right iliac vessels after successful percutaneous transluminal balloon angioplasty of the external iliac occlusion.
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