==== Front EJVES Short RepEJVES Short RepEJVES Short Reports2405-6553Elsevier S2405-6553(18)30026-410.1016/j.ejvssr.2018.06.001Case ReportManagement of Endurance Athletes with Flow Limitation in the Iliac Arteries: A Case Series Khan Assad Al-Dawoud Marwan Salaman Robert Al-Khaffaf Haytham haytham.al-khaffaf@elht.nhs.uk∗Department of Vascular Surgery, East Lancashire Hospitals NHS Trust, Royal Blackburn Teaching Hospital, Blackburn, UK∗ Corresponding author. Department of Vascular Surgery, East Lancashire Hospitals NHS Trust, Royal Blackburn Hospital, Haslingden Road, Blackburn BB2 3HH, UK. haytham.al-khaffaf@elht.nhs.uk20 7 2018 2018 20 7 2018 40 7 11 18 3 2018 15 6 2018 18 6 2018 © 2018 The Authors2018This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).Introduction Vascular surgeons increasingly encounter flow limitation of iliac arteries (FLIA) in endurance athletes. An experience of managing this condition is reported. Report This is a retrospective cohort analysis of prospectively collected data at a single vascular centre. Between 2001 and 2017, 12 athletes with exercise induced pain underwent investigation and assessment. Patients with significant radiological findings (iliac kinking ± stenosis demonstrated on duplex ultrasound or catheter angiography) and dynamic flow changes (marked reduction in ankle brachial pressure indices following exertion, or increase in the common iliac artery peak systolic velocity during hip flexion on duplex) underwent surgery after trialling conservative management; the majority were open iliac shortening procedures. Patients with radiological findings, but no dynamic flow changes were managed conservatively. All patients were followed up. Discussion There were 10 men and two women with a median age of 40 years. Nine patients had iliac kinking (five in isolation, four associated with stenosis), two had stenosis, and one had no iliac disease. Eight patients had severe symptoms (absolute loss of power on maximal exertion) demonstrated dynamic post-exertional flow changes. Seven patients successfully underwent surgery, returning to their sport at similar intensity. One procedure was abandoned owing to severe adhesions from a prior procedure. This patient subsequently changed sport. Three patients with mild symptoms (two had reduction in power at maximal intensity, one was an incidental finding) and who demonstrated no clinical signs of FLIA continued their sport at a lower intensity. Kinking of the iliac arteries in athletes can occur with or without of iliac stenosis. Patients with the most severe iliac symptoms demonstrate dynamic post-exertional flow limitation and may benefit from surgery following a period of conservative management. Patients who have milder symptoms and no dynamic exercise flow limitations can be managed conservatively. Highlights • This series looks at iliac kinking as a cause of flow limitation in iliac arteries (FLIA) of athletes. • Iliac kinking is often overlooked in favour of endofibrosis. • The data demonstrate that iliac kinking can result in FLIA. • Some of these patients would benefit from surgery, after trailing conservative management. Keywords AthletesEndofibrosisFLIAIliac diseaseIliac kinking ==== Body Introduction Pain, loss of power, and/or cramp at maximal effort that resolves upon resting are established as symptoms of underlying flow limitations in the iliac arteries (FLIA).1 Chevalier et al. first suggested that non-atherosclerotic disease could be the cause of FLIA in athletes, owing to vessel stenosis caused by endofibrosis or kinking of the iliac artery, or a combination of both.2, 3 The pathogenesis of the condition typically affects cyclists because of the hyperflexed hip in the cycling position, followed by aggressive and repetitive flexion and extension. This motion stretches the iliac artery, leading to iliac kinking and can result in FLIA.2, 4, 5, 6 Repeated trauma produces a cellular response due to increase in haemodynamic load on the vessel wall, provoking intimal thickening causing stenosis, described as “endofibrosis”.7 In such patients, physical examination and conventional investigations are often normal and provocative tests may be required.8 This paper reports an experience in the diagnosis and management of several athletes suffering disease of the iliac arteries. Design This is a retrospective cohort analysis of prospectively collected data involving all patients experiencing FLIA referred to a single vascular service, managed by the senior authors between the years of 2001 and 2017. Materials and methods Patients were included if they participated in sports competitively and had symptoms of claudication or loss of power during high intensity exercise with resolution upon resting. Patients were excluded if they had other comorbidities contributing to arterial disease or atherosclerosis in other vascular territories. All patients, except one, were assessed using provocative tests, in the form of pre- and post-exercise ankle brachial pressure indices (ABPI) performed on a static exercise bike for cyclists, and treadmill at 5.4 miles per hour at a 15% incline for the single runner in the series. The iliac arteries were radiologically assessed by both duplex ultrasound (DUS) and conventional catheter angiography (via contralateral femoral puncture) with the leg extended and in 90° hip flexion (Fig. 2). Patients were discussed in a multidisciplinary team meeting; patients who demonstrated “symptomatic FLIA”, i.e., a significant iliac tortuosity or stenosis demonstrating flow limitation on post-exercise ABPI, proceeded to surgery after a trial of conservative measures. Patients were extensively counselled about the risks of the procedure, including pseudoaneurysm formation, graft infection (where appropriate), disease progression/recurrence, and limb loss.Figure 1 Operative technique. (a) Open approach (via a Rutherford Morison incision) to the common iliac artery demonstrating iliac kinking even with the patient supine and the hip extended. (b) Excision of the iliac artery. Anastomosis between the two ends displays no tortuosity. Figure 1Figure 2 Pre- and post-operative catheter angiography demonstrating the presence of iliac kinking without stenosis. (a) Angulation without vessel calibre change. (b) Post-operative reduction in angulation with no appreciable difference in diameter. Figure 2 The preferential surgical technique was open iliac artery excision with a spatulated end to end anastomosis (Fig.1a and b). Patients with hostile anatomy underwent ilio-femoral “jump” bypass grafts using Dacron. All patients, irrespective of management, were followed up in the vascular clinic. Results Twelve patients (median age 40 years; 10 men [83%] and two women [17%]) were included in the study; 11 were cyclists (92%) and one was a runner (8%). Eleven patients suffered with limiting symptoms; eight patients (67%) experienced severe symptoms (absolute loss of power at maximal exertional intensity): four in the left leg, two in the right leg, and one in both legs. Three patients (25%) suffered with less severe symptoms (a reduction in power on exertion), allowing them to continue cycling, and one patient was asymptomatic (8%). The predominant radiological finding was iliac kinking, which was present in nine patients: five had isolated kinking and four had kinking with associated stenosis. Two people had stenosis in isolation and one patient (8%) had no identifiable arterial disease. Nine patients had no previous intervention for iliac disease (75%); two patients had undergone previous treatment for iliac stenosis but remained symptomatic (17%). One patient previously underwent iliac thrombectomy after a cycling session and had an asymptomatic contralateral kink detected incidentally during angiography. Patients with severe exertional symptoms had a post-exertional ABPI < 1, with the exception of one patient in whom ABPI was not recorded. All patients with less debilitating symptoms had an ABPI > 1 (Table 1).Table 1 Patient demographics, symptoms, radiological findings, pre- and post-operative ankle brachial pressure index (ABPI), type of procedure, histology, and outcomes. Table 1Age (y) Sex Sport Symptoms Radiological findings Previous procedure Pre-operative ABPI Procedure Histology Successful Post-operative ABPI Follow up (y) Outcome 77 M Cycling Bilateral loss of power at max intensity Kinking No 0.52 (R); 0.45 (L) Bilateral iliac shortening No intimal hyperplasia Yes 1.05 (R); 1.08 (L) 7 Return to cycling 39 M Cycling Left leg loss of power at maximum intensity Kinking No 0.74 Left iliac shortening No intimal hyperplasia Yes 1.11 2 Return to cycling 40 M Running Left leg loss of power at maximum intensity Kinking and stenosis No 0.47 Left iliac shortening Intimal hyperplasia Yes 1.27 3 Return to running 28 M Cycling Right leg loss of power at max intensity Kinking and stenosis No 0.65 Right iliac shortening Intimal hyperplasia Yes 1.16 8 Return to cycling 33 M Cycling Right leg loss of power at maximum intensity Kinking and stenosis Iliac endarterectomy 1.08 Right iliac shortening — No—abandoned 1.04 2 Change to running 75 M Cycling Left leg loss of power at maximum intensity Kinking No 0.77 Left iliac shortening No intimal hyperplasia Yes 1.01 7 (ongoing) Return to cycling 27 M Cycling Left leg loss of power at maximum intensity Kinking and stenosis Iliac stents 1.02 Left iliofemoral bypass No intimal hyperplasia Yes 1.21 10 (ongoing) Return to cycling 40 F Cycling Asymptomatic (incidental finding) Kinking Iliac thrombectomy 1.21 — — — — 7 (ongoing) Still cycling 71 M Cycling Right leg reduction in power at maximum intensity Kinking No 1.31 — — — — 1 (ongoing) Cycling for leisure 21 M Cycling Bilateral thigh and back pain on exertion None No 1.26 (R); 1.16 (L) — — — — 1 (ongoing) Cycling for leisure 44 F Cycling Right leg reduction in power at maximum intensity Stenosis No 1.18 — — — — 1 (ongoing) Cycling for leisure 46 M Cycling Left leg loss of power at maximum intensity Stenosis Open ileo-caecectomy — Left iliofemoral bypass — Yes — 2 months (ongoing) Return to cycling Note. M = male; R = right; L = left; F = female. In terms of management, six patients underwent iliac excision (50%); one had bilateral disease treated and thus seven arteries were treated. One procedure was abandoned because of adhesions around the iliac artery from previous surgery. Two patients underwent an iliofemoral bypass because of hostile anatomy (one patient had iliac stenting and one had an open ileo-caecectomy for complicated appendicitis). From the histology specimens available, five affected arteries demonstrated no evidence of intimal hyperplasia and two showed changes in keeping with endofibrosis. Four patients had no procedure and were managed conservatively. All successfully completed procedures resulted in marked improvements of the post-exertional ABPI (Table 1). One patient in whom the procedure was abandoned showed no significant change in the pre- or post-procedural ABPI; the peak systolic velocity (PSV) in the affected iliac artery during hip flexion remained elevated. Their symptoms still persisted and they subsequently changed their primary sport to running. Three patients managed conservatively reduced the intensity of their cycling. One patient who had an incidental kink continued to cycle at normal intensity. Discussion In this series, patients broadly fall into two categories: those with symptoms, radiological findings, and dynamic flow changes on provocation; and those without dynamic flow changes following provocative tests. ABPI before and after exertion is one of the most accurate diagnostic tools to demonstrate a flow limitation.9, 10, 11 DUS has also been shown to be effective in determining iliac pathology in symptomatic athletes; a significant increase in the PSV during hip flexion reliably correlates with symptoms.12, 13 Patients in whom the ABPI was normal have been managed conservatively and have experienced a reasonable outcome, as all have returned to cycling, albeit at a lower intensity. Conservative management is first line and consists of advice to reduce or stop provocative activities; however, this is only postulated to reduce disease progression.13 Patients with a reduction in ABPI went onto have surgery with good results; 100% of patients that had a successful procedure with documented ABPIs returned to the sport of their choice at a similar intensity. After a minimum of 2 years follow up, none have experienced any recurrence of symptoms or need for re-intervention. Most patients in the series had iliac kinking without endofibrosis (and with in some cases). Despite the lack of intimal hyperplasia, these patients have still been symptomatic, suggesting that iliac kinking alone can result in FLIA.12 While this finding is at odds with the INSITE consensus opinion,14 isolated iliac kinking has still affected the performance of the athletes in our series. Two patients provide credence to this notion. Both had iliac kinking and endofibrosis, and received previous treatment for endofibrosis; one patient had an iliac endarterectomy and the other received iliac stents. Despite having the endofibrosis treated, both patients remained symptomatic and required iliac artery shortening. Iliac stenting has less long-term efficacy, which could have resulted in suboptimal treatment of endofibrosis;13, 14, 15, 16 however, the histology on this patient demonstrated no evidence of endofibrosis and therefore it was iliac kinking alone that was responsible for the patient's symptoms. While the INSITE opinion is not being contested, the present authors would like to make it apparent that iliac kinking in isolation can and does affect athletes independently of endofibrosis,2, 4, 5, 6, 12 and individuals presenting to the vascular surgeon should be assessed on an individual basis; if there is a stenosis or a kink or both causing a marked post-exertional drop in ABPI or a significant increase in the PSV during hip flexion, surgery may be indicated following a trial of conservative measures, provided patients are adequately counselled about the serious consequences and complications of intervention. Two patients underwent an iliofemoral bypass procedure using Dacron. Both made a good recovery and resumed competitive cycling post-operatively. While management preferentially consisted of iliac excision and primary anastomosis, iliofemoral bypass grafts were an acceptable alternative in patients with unfavourable anatomical constraints; they maintain superior patency and limb salvage rates over endovascular treatment,17 and are efficacious in younger patients and athletes.18, 19 Conclusions Competitive athletes, particularly cyclists are susceptible to FLIA. Those who have radiologically demonstrable iliac artery disease and become symptomatic after provocative exertional testing may benefit from surgery after a trial of conservative measures; those without changes after provocative tests should be managed conservatively. Iliac excision and primary anastomosis can result in good functional outcomes. Iliofemoral bypasses are an alternative surgical option in patients whose anatomy is unfavourable with reasonable long-term results. Conflict of interest None. Funding None. ==== Refs References 1 Schep G. Bender M.H. Kaandorp D. Hammacher E. De Vries W.R. Flow limitations in the iliac arteries in endurance athletes. Current knowledge and directions for the future Int J Sports Med 20 1999 421 428 10551336 2 Schep G. Bender M.H. Van de Tempel G. Wijn P.F. De Vries W.R. Eikelboom B.C. Detection and treatment of claudication due to functional iliac obstruction in top endurance athletes: a prospective study Lancet 359 2002 466 473 11853791 3 Chevalier J.M. Enon B. Walder J. Barral X. Pillet J. Megret A. Endofibrosis of the external iliac artery in bicycle racers: an unrecognized pathological state Ann Vasc Surg 1 1986 297 303 3504340 4 Schep G. Kaandorp D.W. Bender M.H. Weerdenburg H. van Engeland S. Wijn P.F. Magnetic resonance angiography used to detect kinking in the iliac arteries in endurance athletes with claudication Physiol Meas 22 2001 475 11556668 5 Schep G.O. Kaandorp D.W. Bender M.H. Van S.E. Weerdenburg H. Titulaer B.M. Excessive length of iliac arteries in athletes with flow limitations measured by magnetic resonance angiography Med Sci Sports Exerc 34 2002 385 393 11880799 6 Schep G. Schmikli S.L. Bender M.H. Mosterd W.L. Hammacher E.R. Wijn P.F. Recognising vascular causes of leg complaints in endurance athletes. Part 1: validation of a decision algorithm Int J Sports Med 23 2002 313 321 12165881 7 Rousselet M.C. Saint-Andre J.P. L'Hoste P. Enon B. Megret A. Chevalier J.M. Stenotic intimal thickening of the external lliac artery in competition cyclists Hum Pathol 21 1990 524 529 2338332 8 Schep G. Bender M.H. Schmikli S.L. Mosterd W.L. Hammacher E.R. Scheltinga M. Recognising vascular causes of leg complaints in endurance athletes. Part 2: the value of patient history, physical examination, cycling exercise test and echo-Doppler examination Int J Sports Med 23 2002 322 328 12165882 9 Abraham P. Chevalier J.M. Leftheriotis G. Saumet J.L. Lower extremity arterial disease in sports Am J Sports Med 25 1997 581 584 9240995 10 Abraham P. Bickert S. Vielle B. Chevalier J.M. Saumet J.L. Pressure measurements at rest and after heavy exercise to detect moderate arterial lesions in athletes J Vasc Surg 33 2001 721 727 11296323 11 Abraham P. Saumet J.L. Chevalier J.M. External iliac artery endofibrosis in athletes Sports Med 24 1997 221 226 9339491 12 Schep G. Bender M.H. Schmikli S.L. Wijn P.F. Color Doppler used to detect kinking and intravascular lesions in the iliac arteries in endurance athletes with claudication Eur J Ultrasound 14 2001 129 140 11704430 13 Peach G. Schep G. Palfreeman R. Beard J.D. Thompson M.M. Hinchliffe R.J. Endofibrosis and kinking of the iliac arteries in athletes: a systematic review Eur J Vasc Endovasc Surg 43 2012 208 217 22186674 14 Hinchliffe R.J. D'Abate F. Abraham P. Alimi Y. Beard J. Bender M. Diagnosis and management of iliac artery endofibrosis: results of a delphi consensus study Eur J Vasc Endovasc Surg 52 2016 90 98 27209899 15 Giannoukas A.D. Berczi V. Anoop U. Cleveland T.J. Beard J.D. Gaines P.A. Endofibrosis of iliac arteries in high-performance athletes: diagnostic approach and minimally invasive endovascular treatment Cardiovasc Intervent Radiol 29 2006 866 869 16565800 16 Wijesinghe L.D. Coughlin P.A. Robertson I. Kessel D. Kent P.J. Kester R.C. Cyclist's iliac syndrome: temporary relief by balloon angioplasty Br J Sports Med 35 2001 70 11157467 17 Indes J.E. Pfaff M.J. Farrokhyar F. Brown H. Hashim P. Cheung K. Clinical outcomes of 5358 patients undergoing direct open bypass or endovascular treatment for aortoiliac occlusive disease: a systematic review and meta-analysis J Endovasc Ther 20 2013 443 455 23914850 18 Radak D. Babic S. Ilijevski N. Jocic D. Aleksic N. Gajin P. Surgical reconstruction for unilateral iliac artery lesions in patients younger than 50 years Vasa 40 2011 474 481 22090181 19 Falor A.E. Zobel M. de Virgilio C. External iliac artery fibrosis in endurance athletes successfully treated with bypass grafting Ann Vasc Surg 27 2013 1183–e1