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provided by Elsevier - Publisher Connector Eur J Vasc Endovasc Surg (2009) 37, 213e220

REVIEW Entrapment Syndromes

A. Noorani, S.R. Walsh, D.G. Cooper, K. Varty*

Cambridge Vascular Unit, Addenbrooke’s Hospital, Cambridge University Hospitals NHS Foundation Trust, Cambridge, UK

Submitted 3 June 2008; accepted 27 October 2008 Available online 1 December 2008

KEYWORDS Abstract Entrapment syndromes represent a pathological process that vascular specialists Superior mesenteric encounter infrequently. However symptomatic patients are often young with impaired quality compression; of life and successful treatment can produce great benefit, making knowledge of these condi- Coeliac artery tions essential. compression; The purpose of this review was to bring together the entrapment syndromes to understand Popliteal artery and gain consensus on the aetiology, pathogenesis, diagnosis and modern management of entrapment; these rare and interesting vascular disorders. This includes entrapment syndromes of the popli- Iliac compression; teal artery, superior mesenteric artery, coeliac artery, and iliac vein. May Thurner’s; ª 2008 European Society for Vascular Surgery. Published by Elsevier Ltd. All rights reserved. Nutcracker syndrome

Introduction quality of life and successful treatment can produce great benefits. Most modern vascular practice encompasses atheroscle- rotic arterial disease and venous insufficiency. External Methods compression of normal vessels represents a different and infrequent pathology. The best known is thoracic outlet The Pubmed and Medline databases were searched from 1 syndrome, which was recently reviewed. This review 1966 to 2007 to identify articles relating to vascular focuses on the remaining compression syndromes as entrapment syndromes. The terms ‘popliteal entrap- shown in Fig. 1. Compression syndromes can cause ment’, ‘superior mesenteric artery syndrome’, coeliac ischaemia (arterial or visceral entrapment) or stasis artery entrapment’, ‘iliac vein entrapment’, ‘May Thurn- (venous entrapment). Many patients are asymptomatic er’s’, ‘nutcracker’ and ‘renal vein entrapment’ were but symptomatic patients are often young with impaired used.

* Corresponding author. K. Varty MD, FRCS, Consultant Vascular Surgeon, Level 7, Box 201, Addenbrooke’s Hospital, Hills Road, Cambridge CB2 2QQ, UK. Tel.: þ44 1223 217246; fax: þ44 1223 216015. E-mail address: [email protected] (K. Varty).

1078-5884/$34 ª 2008 European Society for Vascular Surgery. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.ejvs.2008.10.019 214 A. Noorani et al.

ENTRAPMENT SYNDROMES

ARTERIAL VENOUS VISCERAL Subclavian Artery Iliac Vein (May Thurner) Superior Mesenteric Artery Popliteal Artery Renal Vein (Nutcracker) Syndrome (Wilkie) Coeliac Artery

Figure 1 Categorisation of entrapment syndromes.

Results popliteal artery and retardation of varying degrees of the pathway of migration of the medial head of gastrocnemius Popliteal artery entrapment syndrome results in the first two types of entrapment (Table 1). Unlike anatomical popliteal entrapment, functional popliteal entrapment (type 6) occurs in patients with Popliteal artery entrapment syndrome (PAES) results from unremarkable popliteal anatomy.14 This is associated with an abnormal anatomical relationship between the popliteal gastrocnemius hypertrophy as seen in athletes and patients artery and its surrounding musculotendinous structures. using anabolic steroids which can cause intermitted First described in 1879,2 the first operative treatment was compression of the popliteal artery on plantar flexion.15,16 reported 80 years later (medial head of gastrocnemius myotomy and popliteal artery endarterectomy).3 Diagnosis and investigations Patients present with claudication, calf swelling and Epidemiology paraesthesia. Active knee hyperextension followed by PAES predominantly affects young men (male:female ratio 17 e plantar flexion may or may not attenuate foot pulses and 9:1) lacking atherosclerotic risk factors.4 6 The true inci- is not a reliable diagnostic test. On duplex, decreased peak dence is unknown. 3.8% of post-mortem limbs have aber- systolic activity on active plantar flexion against resistance rant anatomy consistent with PAES.5 A prevalence of 0.165% or knee flexion to 15 degrees is considered diagnostic.18 in Greek soldiers suggests that clinically significant PAES is However popliteal artery occlusion on stress manoeuvres is less common than the anatomical abnormality.6 PAES is reported in the order of 59e85% of asymptomatic patients, responsible in 60% of young patients with ischaemic pain.7 indicating a significant false positive rate with duplex.19,20 Unilateral PAES should prompt contralateral investigation6 Angiography is the classical investigation for PAES. as bilateral PAES is reported in 22e67%.7 Popliteal artery compression under plantar flexion at angiography strongly indicates PAES (Fig. 2). It may Pathophysiology demonstrate medial deviation of the artery in 24% of all Recurrent popliteal artery compression causes intimal cases, indicative of type 1 PAES. Alternatively it may damage, , distal embolisation,8 post-stenotic demonstrate or ectasia in 9%, and occlusion in dilation and true aneurysm formation, seen in 13.5% of all 36% on dynamic manoeuvres, or irregularity of wall in the cases.9,10 Unlike , entrapment features presence of normal arterial vasculature.21 Angiography neovascularisation, inflammatory cell infiltrate and vessel allows assessment of the distal vasculature for embolisa- wall disruption, stimulating fibrosis and collagenisa- tion22 but cannot differentiate atherosclerosis from tion.11,12 Once aneurysm or thrombus formation occurs, arterial damage is irreversible.11

Embryology and classification Table 1 Classification of popliteal entrapment syndrome The types of popliteal artery entrapment are differentiated Type 1 Popliteal artery medially displaced, normal MHG on an anatomical basis (Table 1) and are better understood Type 2 Normal popliteal artery, laterally displaced MHG 13 in the context of embryological development. The prox- Type 3 Compression of popliteal artery imal popliteal artery results from the fusion of the ischiadic by additional slip of gastrocnemius artery and the developing femoral arterial plexus, whilst Type 4 Compression of popliteal artery by popliteus the mid-portion is derived from the axial artery. The distal Type 5 Compression of popliteal vein12 third of the popliteal artery is only formed from the fusion Type 6 Functional entrapment of popliteal of the anterior and posterior tibial once the medial artery. No aberrant anatomy head of gastrocnemius migrates to occupy a medial position MHG: medial head of gastrocnemius. in the popliteal fossa. Premature formation of the distal Entrapment Syndromes 215

Figure 3 CT angiogram demonstrating external compression of the popliteal artery on plantar flexion (arrow pointing to popliteal artery).

and vein patching28 for stenoses with a complication rate of 16.7% compared to 45.5% (p < 0.01).29 Bypass using vein graft remains the treatment of choice for occlusion. Patency rates have been reported at to 57e65% over a period of 8e10 years,30,31 though studies remain limited because of small sample sizes. The posterior approach is preferable for short occlusions, providing excellent visual anatomy, access to the short saphenous vein (for interpo- sition grafting) and better cosmesis.27,32 Longer occlusions are approached medially, as they necessitate a longer bypass graft. Surgery is recommended in all patients with Figure 2 Angiogram showing complete occlusion of the left anatomical PAES and symptomatic cases of functional and partial occlusion of the right popliteal artery on plantar entrapment syndrome. Surgery in asymptomatic cases of flexion. functional popliteal entrapment is not justified as these patients are not at an increased risk of vascular 33e36 anatomical entrapment in patients with occlusion. complications. Computed tomographic angiography (CTA) (Figs. 2 and 3) and magnetic resonance angiography (MRA) can demon- Coeliac artery compression syndrome strate popliteal artery and musculotendinous anatomy, and identify other pathology, e.g. adventitial cysts that mimic Coeliac artery compression syndrome (CACS) results from PAES.23 MRA, though expensive, is equivalent to digital extrinsic compression by the median arcuate ligament or subtraction angiography, and can clearly distinguish func- ganglionic tissue of the coeliac plexus.37 Aberrant anatomy, tional and anatomical PAES.24e26 e.g. a high coeliac origin or low diaphragmatic crus may contribute. Some dispute the existence of CACS suggesting Management that collaterals should prevent ischaemic symptoms and Definitive management requires surgery to release extrinsic positive surgical outcomes result from coeliac plexus tran- compression and preserve or restore arterial flow. If arte- section, not coeliac artery decompression.38 Asymptomatic rial damage is minimal, myotomy of the medial head of coeliac artery compression exists in 3e10% of patients gastrocnemius or any abnormal musculotendinous slips may undergoing liver transplantation.39 The diagnosis of coeliac suffice.27 More severe cases require arterial repair. Inter- artery entrapment syndrome is made on the combined basis position vein grafting outperforms thromboendarterectomy of clinical and radiological findings. 216 A. Noorani et al.

Diagnosis and investigations increasingly popular imaging choices.64 The gold standard is Symptoms include weight loss, , , diarrhoea retrograde venography and (cine-video angiography) with and postprandial pain, usually epigastric.40,41 Some have an reno caval pressure gradient measurements. Cine-video expiratory systolic bruit.37,40 Athletes report exercise- angiography illustrates precisely the point of left renal vein related symptoms. Occasionally, cause coeliac compression and demonstrates reflux of contrast into plexus irritation, mimicking CACS.42 Mitral valve prolapse the adrenal and gonadal from peri-ureteral and peri- and pancreatico-duodenal aneurysms have also been renal venous collaterals, and pooling of contrast into reported in association with CACS.43,44 Mesenteric duplex the renal vein. The gradient between the scanning is the initial investigation of choice, followed by left renal vein and IVC needs to exceed 3 mmHg to make CTA or MRA. Biplane angiography can highlight worsening the diagnosis.65 coeliac artery compression on inspiration. Gastric tonom- etry may reveal gastric ischaemia45 and has been advocated Management as exercise precipitates ischaemia in 86% of patients with Surveillance is a reasonable option in minimally symptom- known splanchnic .46 Tonometry normalised in all atic young patients. In particular, this is applicable to patients who were asymptomatic following surgery, pubertal patients because of a higher rate of spontaneous compared to only 25% of patients who remained symp- remission, possibly due to physical development.66 Surgical tomatic despite intervention.47 options include transposition of the renal vein further down the IVC 54,67 or the SMA caudally on the , though this Management has a higher risk of complications.60 Auto transplantation of Transection of the median arcuate ligament and diaphrag- the affected into the iliac fossa may achieve good matic crus proximal to the artery followed by neurolysis results.64,68 Gonadal caval bypass has been described for and transection of the ganglionic tissue relieves symp- cases with extensive pelvic varices, but the results are not toms.48 Additional coeliac artery dilatation or interposition encouraging.60 Intravascular stents have achieved good grafting improves outcomes, suggesting that decompression initial results, though long term follow-up is required.69e73 alone is not always sufficient.45 Laparoscopic decompres- Extravascular stenting involves placing PTFE graft around sion achieves good results when combined with endovas- the renal vein, either at laparotomy70 or laparoscopically.60 cular methods to dilate the artery.49,50 Endovascular Management of the nutcracker syndrome may resolve stenting without surgical decompression has limited long haematuria, though pressure measurements may fail to term benefit because of continual extrinsic compression reflect this improvement.56 resulting in re-stensosis and fracture. Data remains limited because of the rarity of the condition.51,52 MayeThurner syndrome

Nutcracker syndrome Compression of the left common iliac vein between the right common iliac artery anteriorly, and the fifth lumbar This describes left renal vein entrapment between the SMA vertebra posteriorly can cause stasis and lower limb deep and aorta. The renal vein can be compressed if the SMA vein thrombosis, accounting for the increased incidence of emerges more acutely, from a lower or lateral aortic origin, left sided DVT.74 May and Thurner analyzed autopsy speci- or descends caudally after a shorter than normal distance mens and found ‘intraluminal-spurs’ at the junction of the of 4e5 mm.53,54 Rarely the left renal vein passes behind the left common iliac vein (LCIV) with the IVC in 22% of aorta where it is compressed against vertebrae, causing subjects. They proposed that these were predisposing posterior nutcracker syndrome.55 Anterior and posterior factors for ileo-femoral DVT75 and arose from chronic nutcracker syndrome can occur simultaneously.56 intimal damage of the LCIV secondary to pulsatile move- ment of the right common iliac artery. Absence of spurs in Clinical features fetal autopsies suggests they are acquired, not congen- Renal vein compression causes renal , disrup- ital.76 Cockett and Thomas correlated the clinical features tion of small renal veins and consequent rupture into the of this condition with its pathological findings, calling it collecting system, manifesting as micro- or macro-haema- ‘iliac compression syndrome’.77 Eponymous names are turia.57 Patients present with flank or non-specific abdom- MayeThurner or Cockett’s Syndrome. inal pain and nausea and vomiting. Reflux from the left renal vein to the left gonadal vein can result in testicular Clinical features pain and varicocoele formation.58 Some develop pelvic It typically affects young and middle aged women75 and congestion syndrome with genital, pelvic and thigh varices, may contribute in 18e49% of patients with left sided dysmenorrhoea, dyspareunia, post coital ache and lower DVT.78,79 Symptoms include lower limb swelling and pain in .59,60 Nutcracker syndrome mainly affects the acute stage, and , venous eczema, females in third and fourth decades. The precise incidence hyperpigmentation, exertional pain and venous ulcers in is unknown, though diagnostic features may be present on the chronic stage (post-thrombotic limb).80 Conventional 72% of CT scans.61 Duplex sonography has a sensitivity of venography delineates pelvic vein anatomy, collateral 78% and a specificity of 100%.62 It compares measurements formation and iliac vein compression with consequent spur of peak velocity and renal vein diameter at the renal hilum formation (Fig. 2). May and Thurner advised the use of iliac and where the SMA crosses the renal vein. A five-fold ratio vein pressure differences (2 mm and rest and 3 mm on is highly indicative of the diagnosis.63 CTA and MRA allow exercise) as diagnostic criteria.75 MR Venography (MRV) is visualisation of the renal vein and SMA anatomy, and are the preferred imaging modality, as apart from its diagnostic Entrapment Syndromes 217 accuracy it illustrates any external compression by intra- Table 2 Additional factors triggering SMAS abdominal pathology.81 Causes Examples Management Aberrant anatomy High insertion of Anticoagulation alone is insufficient, failing to relieve the (congenital) ligament of Treitz underlying mechanical compression. Compression Low SMA origin bandages or stockings have benefits but are unpopular. Trauma and the Burns,87 prolonged ITU stay90 Multiple surgical approaches have been described catabolic state 82 including thrombectomy in the acute stage. Vein patch Intra-abdominal compression Peritoneal adhesions91 angioplasty with intra-luminal band excision and/or Extra-abdominal compression Spica casts92 interposition of a fascia lata sling or a peritoneal flap can Surgical procedures Spinal fixation,93 be performed to avoid recurrent damage. The right ileo-anal anastomosis94 common iliac artery can be relocated behind the LCIV or Weight loss Anorexia,97 malabsorption, IVC. Finally a Palma Crossover procedure can be per- cardiac cachexia98 formed. Success remains variable, with 40e88% patency Local factors Aneurysm,98 neoplasm rates of the commmon iliac vein or venous bypass.79,82 None of the surgical options demonstrates clear superi- ority. Catheter-directed thrombolysis followed by angio- plasty with stent placement has recently been Clinical features reported.83,84 Mickley et al. placed percutaneous stents Presenting features include postprandial discomfort, intraoperatively on the finding of venous spurs in radio- nausea, weight loss and early satiety. The pain is typically logically proven cases of MayeThurner’s Syndrome. The relieved in the lateral decubitus position or by bringing the re-occlusion rate in patients with stents following knees to the chest which reduces tension on the small thrombectomy was 13% compared to 73% in the group bowel mesentery. Barium studies demonstrate a dilated which was thrombectomized alone.78 proximal duodenum terminating at the third part. Four criteria differentiate SMAS from megaduodenum: 1) dila- Superior mesenteric artery syndrome tation of the first and second parts of the duodenum with or without gastric dilation 2) reverse flow of contrast proximal Superior mesenteric artery syndrome (SMAS) is obstruction to the obstruction 3) 4e6 h delay in contrast transit 4) of the third part of the duodenum (D3) secondary to obstruction relieved in the prone knee-chest or lateral external compression by the SMA. First described by Von decubitus position.95,96 Rotikansky in 1842,53 it is also referred to as Wilkie Doppler imaging may reveal a reduced aorto-mesenteric syndrome,85 cast syndrome or arterio-mesenteric angle.95 CTA or MRA may identify a reduced aorto-mesen- duodenal compression.86 SMAS may be confused with teric angle, or contributory local pathology, e.g. aneurysm megaduodenum, though the latter differs by character- or neoplasia. Angiography remains the gold standard istic dilation of the duodenum without proximal stenosis investigation. An aorto-mesenteric angle less than 22e25 and is secondary to cases of intestinal myopathy. Barium degrees and a distance of less than 8 mm is used as studies demonstrate SMAS in 0.13e0.3% of the pop- a threshold for diagnosis.95 All patients require an oeso- ulation.87 It is more common following scoliosis surgery phagogastroduodensocopy to exclude peptic ulcer (0.5e2.4%)88,89 and in severely burned patients (1.1%).90 disease.99 Typically, it affects women and 75% are between 10e39 years of age.91 Management Medical management is the mainstay. Gastroduodenal Pathophysiology decompression, hyperalimentation and correction of The SMA normally forms an angle of between 38 and 60 contributing conditions aim to restore retroperitoneal degrees at its aortic origin.85,87 The arterio-mesenteric tissue bulk and hence the aorto-mesenteric angle. Nutrition distance ranges from 10 to 28 mm.87,92 This angle is is provided by nasogastric feeding, or ideally by a nasoje- maintained by retroperitoneal tissue, the left renal junal tube placed distal to the obstruction.99 Total paren- vein, lymphatic tissue and the pancreatic uncinate teral nutrition is a useful adjunct or an alternative if process. A decrease in this angle to 6e16 degrees or the enteral feeding is impossible. Metoclopramide may mean arterio-mesenteric distance to 2e8 mm results in the enhance motility. Non-operative treatment has a success artery compressing D3.87,92 Thin body habitus may predis- rate of 83%.96 Surgical care is warranted when medical pose to SMAS but an additional insult is required for the management has been unsuccessful, especially in patients condition to manifest (Table 2). Catabolic and malnour- with chronic SMA syndrome with duodenal stasis and ished states predispose to this condition by a reduction in complicating peptic ulcer disease. Gastrojejunostomies mesenteric and retroperitoneal fat, hence the increased provide gastric decompression but may not alleviate risk in patients with burns.90 All patients requiring pro- duodenal obstruction, causing persistent symptoms. Divi- longed bedrest following severe injury are at risk.93 sion of the ligament of Treitz with duodenal mobilisation Lengthening of the spine during scoliosis surgery88,89 and (Strong’s procedure) has also been carried out, though it caudal pull on the mesentery during ileo-anal anasto- may lead to volvulus. A duodenojejunostomy remains the mosis94 reduces the aorto-mesenteric angle, leading to operation of choice to relieve the obstruction, with success SMAS. rates up to 90%,87 though it may cause blind loop syndrome. 218 A. Noorani et al.

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