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Radiology and mesenteric ischaemia
Clinical Radiology 70 (2015) 698e705
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Clinical Radiology journal homepage: www.clinicalradiologyonline.net
Review
Radiology and mesenteric ischaemia E. McCarthy, M. Little, J. Briggs, J. Sutcliffe, C.R. Tapping, R. Patel, M.J. Bratby, R. Uberoi* Oxford University Hospitals, Department of Radiology, John Radcliffe Hospital, Headley Way, Headington, Oxford, OX3 9DU, UK
article in formation Article history: Received 18 December 2013 Received in revised form 29 October 2014 Accepted 17 February 2015
This review focuses on the radiology of mesenteric ischaemia. Covering the acute and chronic presentations, both of which result from impaired vascularisation of the gastrointestinal tract, we evaluate the role of radiographs, ultrasound, CT, MRI, and catheter angiography in the diagnosis of these conditions. Looking to the future, we also assess some of the emerging imaging techniques. Across medicine and surgery there has been a significant shift towards minimally invasive interventions. Although percutaneous revascularisation of chronic mesenteric ischaemia has been performed for some time, there has been a developing trend for the use of such techniques in acute mesenteric ischaemia. We evaluate the available evidence for the use of these percutaneous interventions and assess how they compare with or in some instances compliment traditional surgical alternatives. Ó 2015 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
Introduction
AMI
Mesenteric ischaemia encompasses both acute and chronic conditions resulting from impaired blood flow to the intestines. Acute mesenteric ischaemia (AMI) is a lifethreatening event that requires prompt identification and treatment. Chronic mesenteric ischaemia (CMI) is a more insidious entity, often a diagnosis of exclusion, presenting with progressive cachexia and reproducible post-prandial pain. In this review, we focus on the radiological investigations being employed in current clinical practice and those in evolution. We also evaluate the role of imageguided interventions and how they compare with and compliment the surgical alternatives.
AMI is a rare but life-threatening condition requiring prompt identification and treatment. AMI has a mortality ranging between 30 and 90% dependent on aetiology and time to intervention.1 Time at presentation is a crucial factor. Animal studies carried out by Udassin et al.2 demonstrated the effects of absolute ischaemia on the mucosal lining of the small intestine. Structural changes of the villi were identified at 15 minutes with trans-mural necrosis and gangrene identified at 6 hours2. The aetiology of AMI can be divided into occlusive, and non-occlusive causes (Table 1). Occlusive disease accounts for 85% of presentations: in situ arterial thrombosis in 50%, including dissection (Fig 1); embolic thrombus in approximately 20%; and mesenteric venous thrombosis in 15%.3 Atherosclerotic plaque has a predilection for the vessel ostiae with ulceration of these plaques leading to thrombosis. Although atherosclerotic plaque does not demonstrate predilection for any particular vascular territory, 50%
* Guarantor and correspondent: R. Uberoi, Oxford University Hospitals, Department of Radiology, John Radcliffe Hospital, Headley Way, Headington, Oxford, OX3 9DU, UK. Tel.: þ44 (0) 01865 741166; fax: þ44 (0) 01865 220801. E-mail address: [email protected] (R. Uberoi).
http://dx.doi.org/10.1016/j.crad.2015.02.012 0009-9260/Ó 2015 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
E. McCarthy et al. / Clinical Radiology 70 (2015) 698e705
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Table 1 Causes of acute mesenteric ischaemia. Occlusive
Non-occlusive
Arterial occlusion
Hypovolaemia
Thromboembolic disease Dissection Venous thrombosis
Cardiogenic/hypovolaemic shock Transection Vasoconstriction
Hyper-coagulable state Recent surgery Abdominal sepsis Portal hypertension Mechanical compression
Ergot alkaloids Cocaine Vasculitides
of occlusive arterial embolic episodes involve the superior mesenteric artery (SMA; Fig 2). The origin of this vessel usually has a less acute angle than the coeliac artery making it a more likely destination for emboli. Emboli usually lodge distal to the middle colic and jejunal SMA branches with a small proportion lodging proximally at the vessel origin. 20% of patients with SMA emboli will have synchronous embolisation of another arterial bed.4,5 Symptomatic inferior mesenteric artery (IMA) emboli are less frequent given the smaller vessel calibre and the extensive collateralisation from SMA, and middle and inferior haemorrhoidal territories. Non-occlusive causes of AMI account for 15% and are the result of low flow states, such as cardiogenic shock, ergot medications, and trauma.3,6e8 Patients typically present with abdominal pain, nausea, vomiting, and less frequently, bloody diarrhoea. They are likely to have raised C-reactive protein, leukocytosis, metabolic acidosis, elevated D-dimers, can be Figure 2 (a) Axial section from an arterial-phase CT examination demonstrating luminal filling defect in the SMA of a 66-year-old woman who presented with abdominal pain (arrow). No associated bowel wall abnormalities were identified. Features were consistent with acute embolic mesenteric ischaemia. (b) Formal catheter angiography demonstrating a filling defect in the distal main SMA (arrow). (c) This was treated via thrombo-aspiration through a 6 F guide catheter with good angiographic result (arrow).
Figure 1 Type A dissection flap extending into the SMA (arrow) of a 71-year-old man. This flap resulted in thrombosis of a short segment of the proximal SMA. The patient underwent emergent aortic root repair. Despite the SMA dissection flap being documented, the short segment thrombosis was not initially identified leading to small bowel ischaemia in the early postoperative period.
hyperkalaemic, and have a raised lactate.9 Raised lactate is a late finding, associated with concomitant intestinal necrosis and a poor outcome, (sensitivity 90e96%, specificity 60e87%).10 Indeed, although classic descriptions include metabolic acidosis, one prospective clinical trial described a metabolic alkalosis being more common secondary to the profound vomiting associated with this condition.11 Recent clinical reviews have focused on biomarkers for the earlier clinical detection of intestinal ischaemia. These include intestinal fatty acid binding protein (I-FABP) and alphaglutathione S transferase (GST).12e14
Imaging of AMI A variety of imaging techniques have been employed in the evaluation of AMI. Radiography, duplex ultrasound, multi-
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section CT, endoscopy, MRI, and angiography have all been evaluated. Angiography has historically been the reference standard for the diagnosis of AMI, and its introduction initially led to improved diagnosis with better survival rates.15,16 Angiography allows both diagnosis and the potential to carry out therapeutic procedures simultaneously. However, this is not available in all units, is an invasive procedure, and is uncommonly performed in the acute setting. Erect chest radiography and/or plain films of the abdomen are frequently obtained in patients with abdominal pain. Their role in the evaluation of AMI is limited; an abdominal radiograph cannot exclude AMI as 25% of patients with the condition will have a normal abdominal film.17 Bowel obstruction, bowel wall oedema, intraperitoneal free gas, portal venous gas, and pneumatosis intestinalis can be identified at radiography; however, these findings are typically identified late, often when bowel ischaemia/infarction has already developed.18 Ultrasound assessment is usually carried out with lowfrequency curvilinear probes. The coeliac artery and SMA are identified coming off the aorta in the sagittal plane. The IMA is often difficult to visualise. The vessels are interrogated using Doppler mode, which is highly specific (92e100%) but has a lower sensitivity (70e89%) for identifying vascular occlusions. It is less successful in the assessment of non-occlusive thrombus or distal occlusion.15 In the early phase of arterial occlusive AMI, ultrasound may demonstrate SMA occlusion and bowel spasm. In the intermediate phase, ultrasound is less informative due to gaseous accumulation in the bowel with resultant acoustic impedance. Later, fluid-filled loops, decreased or absent peristalsis, bowel wall thinning, or peritoneal free fluid may be seen. In venous occlusive AMI, ultrasound may reveal focal SMV or portal thrombus, decreased peristalsis, increased intraluminal secretions, and segmental mural thickening.19 In advanced cases, intramural gas and portal venous gas may be evident. This technique is helpful in narrowing the differential causes of abdominal pain but actual image quality and reproducibility of results is operator dependent, and in certain instances, can be limited by overlying bowel gas. CT angiography (CTA) has evolved over the past decade and is currently recommended as the first-line imaging technique.15,20 CTA, unlike angiography is widely available and non-invasive. In our institution CTA is performed using a 64 section system (Lightspeed, GE Healthcare, Bucks, UK). The imaging parameters are 0.625 mm collimation, 0.5 pitch, 0.4 seconds rotation speed, 120 kVp, smart tube current, and a soft reconstruction kernel. We use 100 ml iopamidol (370 mg iodine/ml; Niopam 370, Bracco UK, Bucks, UK). Imaging is obtained at 30 seconds with contrast medium administered at a rate of 3 ml/s. Evolution of multi-section CT technology allows the reconstruction of vessels in three-dimensional (3D) planes. Added to that, CT affords the ability to image the gastrointestinal tract for the ancillary findings of AMI. It also allows evaluation of the genitourinary tract for differential diagnoses in the acute abdomen. Many studies document the success of CT in identifying findings suggestive of AMI.19e26
Signs associated with AMI include vascular luminal filling defects or truncation of the vessels, focal lack of mural enhancement, bowel wall thickening, fat stranding, pneumatosis intestinalis, portal venous gas (Fig 3), intraperitoneal free gas, and ascites. Bowel wall thickening is the most frequently observed finding in AMI. It has a high sensitivity (85e88%) but as expected is much less specific (61e72%). Intra-luminal defects or occlusions of the mesenteric vessels are less sensitive (12e15%) but are again highly specific (94e100%). A combination of signs will help increase reader confidence. Combining bowel wall abnormalities (thickening/lack of mural enhancement) with pneumatosis intestinalis increases specificity to between 97 and 100%.22,23,26,27 Paradoxically, hyper-enhancement of the bowel wall can also be an indicator of acute ischaemia. This may be secondary to hyperaemia (from mesenteric venous occlusion or from reperfusion injury.28 Interpretation of pneumatosis intestinalis can be challenging for the reporting radiologist. Pneumatosis intestinalis refers to gas within the wall of the bowel, and a good rule of thumb is to look for intramural gas in the dependent colon. The importance of isolated pneumatosis intestinalis is controversial. Duron et al.29 evaluated a large group of patients with pneumatosis using CT, 47% of their cohort with this finding improved or had negative laparotomies. Lee et al.30 investigated an oncological cohort and found that in patients with cancer, benign pneumatosis (requiring no intervention, that resolved or improved on subsequent imaging) was confined to the colon, whereas clinically worrisome pneumatosis (destined for laparotomy), although being associated with bowel dilatation, stranding, mural thickening, and ascites, was also more likely to be limited to the small bowel. These studies reiterate the importance of considering all imaging findings and the clinical context when considering a diagnosis of AMI. Furthermore, it is important to be able to distinguish benign variants of pneumatosis intestinalis, in particular pneumatosis cystoides intestinalis. The cystoides variant typically presents with sub-mucosal/sub-serosal cyst formation and although
Figure 3 Axial section on lung windows through the abdomen of a 69-year-old woman. Pneumatosis intestinalis (arrow) and gas within an SMV tributary (arrowhead) are demonstrated, features consistent with ischaemic bowel.
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this can also result in pneumoperitoneum, it tends to have a more benign presentation and clinical course. Pneumatosis cystoides is associated with connective tissue disorders, chronic obstructive airways disease, and steroid use. Magnetic resonance angiography (MRA) at 1.5 T has a high sensitivity and specificity for evaluation of occlusions or high-grade stenoses of the proximal coeliac trunk or SMA. It has limited value in the evaluation of distal mesenteric occlusions.31,32 MRA is time consuming and not as freely available as CT, which limits its usefulness in the acute setting. Recent lab based research has examined the possible role of 3 T, 7 T MRI, and positron-emission tomography (PET) in the evaluation of AMI.33e37 Macroscopic, 7 T MRI and histological appearances after ligation of rodent IMA, SMA, and SMV have been evaluated with an encouraging positive correlation between the imaging and histological findings. Abnormalities were identified on imaging as early as 30 minutes post-ligation, progressively worsening until the end point at 8 hours. MRI has the potential to become the imaging method of choice in the future with further technological evolution. Similarly, PET has been able to demonstrate significant reductions in porcine hepatic perfusion (40%), intrahepatic blood content (75%), and portal blood flow (45%) after induced intestinal ischaemia. This reduction in flow and blood content persisted during reperfusion of the intestine.37 Further studies will be required to assess the possible clinical role of PET in AMI imaging.
Image-guided management of AMI Treatment of AMI traditionally involved laparotomy and segmental bowel resection with mesenteric revascularisation via surgical bypass if required. Minimally invasive radiologically guided interventions have been described and can be attempted in the absence of peritonism or imaging findings consistent with perforation. Therapeutic endovascular options include aspiration thromboembolectomy, pharmacological and/or mechanical thrombolysis, antegrade visceral arterial stenting, and hybrid intra-operative retrograde stenting. Percutaneous access is usually obtained via the femoral or brachial artery. Historical data demonstrate higher survival rates when vasodilators have been administered as part of the treatment of AMI.38 To this effect transcatheter papaverine can be used in acute arterial occlusion and in non-occlusive vasospastic AMI. Papaverine is a phosphodiesterase inhibitor that increases circulating intracellular levels of cyclic adenosine monophosphate (cAMP), a vascular smooth muscle relaxant. Papaverine is administered as a bolus dose of 60 mg followed by an infusion (30e60 mg/h) continued for 24e48 hours with repeat angiograms performed every 24 hours. A stable catheter position is required to avoid intra-aortic delivery, which would result in profound hypotension.16,38,39 However, there has been no significant addition to the evidence basis for this therapy over the course of the last 30 years. Catheter thrombo-aspiration is a well-documented approach.40,41 This is usually performed with a long
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arterial sheath placed as close to the luminal obstruction as possible. A wide-bore guide catheter (6e8 F) is repeatedly manoeuvred through the thrombus/embolus while back suction is placed on the catheter using a 20 ml syringe. A number of attempts are usually required to dislodge the obstruction (Fig 2bec). Intra-arterial thrombolytic therapies including streptokinase, urokinase, and tissue plasminogen activator (t-PA) have been described. In one systematic review, 30 of 48 (63%) patients avoided surgery after primary treatment with thrombolytics.42 Intra-arterial thrombolysis has not become a favoured monotherapy due to the time taken to re-vascularise and the potential bleeding risk from the ischaemic mucosa. In clinical practice, a combination of approaches may be required for re-vascularisation; this is where intra-arterial thrombolysis can be quite useful in the treatment of residual clot.43 Recently, the successful use of mechanical and aspirational thrombectomy devices including Aspirex S (Straub Medical, Switzerland), Rotarex S (Straub Medical, Switzerland), Angiojet (Bayer, CA, USA), and Merci Retriever (Concentric Medical, The Netherlands) have been described, all be it in small case series and case reports.44e46 Once the acute luminal obstruction has been treated, there is often an underlying stenosis that needs to be managed, and this can be carried out during the same procedure. Percutaneous transluminal angioplasty of the SMA in AMI has a poor long-term outcome and arterial dissection as a result of angioplasty would render subsequent stenting difficult.45 As such, primary stenting for critically narrowed lesions is the approach of choice. The use of both balloon mounted and self-expanding stents have been described. The more precise balloon mounted approach appears favourable for proximal lesions, whereas the self-expanding stents accommodate distal SMA tortuosity better.47 Seven to 9 mm diameter stents are commonly deployed in the coeliac artery and SMA. Intra-operative retrograde transluminal angioplasty and stenting of the SMA has also been successful. This approach combines endovascular techniques and surgery, allowing assessment and resection of the nonviable bowel.48,49 At the time of laparotomy, an arteriotomy is made in the main trunk of the SMA and a wire is passed retrogradely into the aorta. This is then snared in the aorta via a femoral (or brachial) approach and the wire pulled through. If required, a surgical embolectomy balloon can be passed through the occlusion and the vessel can then be stented. A small retrospective study of 13 patients demonstrated lower in-hospital mortality rates associated with this hybrid approach (17%) compared with surgical bypass (80%) and percutaneous stenting at 100%.49 A recent evidence-based review concludes that postoperative complications and inpatient mortality rates are lower for endovascular therapies than for open surgery and that endovascular thrombolysis prior to open surgery may reduce the length of bowel resected. The evidence is limited and management should be decided on a case-bycase basis.50
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CMI The condition usually occurs in patients over 60 and demonstrates a 3:1 female predominance.51 This is despite the fact that up to 60% of the normal population demonstrate some degree of mesenteric arterial stenosis.52 Patients classically present with epigastric/periumbilical postprandial pain. This pain typically commences 30 minutes post-eating, lasts 1e2 hours and may result in sitophobia (fear of food) with significant consequent weight loss. Traditional descriptions require occlusion or high-grade stenosis of two of the three visceral arteries.53 This is because of the protection provided by presence of a number of collateral pathways within the mesenteric circulation including the pancreatico-duodenal arcade, marginal artery of Drummond, arc of Barkow, arc of Riolan and the arc of Buhler. In CMI, the SMA is the most frequently involved vessel. Isolated stenosis of the SMA resulting in symptoms has been reported.54 Isolated cases of coeliac artery involvement have also been described; however, this is more likely to be the result of median arcuate ligament syndrome. This syndrome typically presents with similar symptoms to CMI, although in a younger population. Median arcuate ligament syndrome occurs due to compression of the coeliac artery and coeliac ganglia by the median arcuate ligament, a fibrous arch formed by the right and left diaphragmatic crura.55 Atherosclerosis is the cause of CMI in the vast majority of cases. Less commonly CMI can be attributed to fibromuscular dysplasia or arcuate ligament syndrome. Rarer causes include; polyarteritis nodosa, Buerger’s disease, Takayasu’s disease, arterial dissection, and abdominal aortic aneurysm.56e58
Imaging of CMI Radiographs have no role to play in the diagnosis of CMI as patients have not developed bowel necrosis, and therefore, the radiograph will likely be normal or demonstrate non-specific findings.15 Unlike in the acute setting, Doppler ultrasound has been more successfully employed in the chronic presentation. This imaging technique has the added benefit of dynamic assessment of flow through anatomically narrowed vessel segments. Duplex is best performed in the fasting state and early in the day to avoid bowel gas.59 Anecdotally the weight loss, which invariably accompanies this condition, should aid sonography, although vessels may remain difficult to visualise. In one study, 83% of coeliac trunks and 93% of SMA vessels were visualised on the initial duplex studies compared with 100% of coeliac trunks and 99% of SMAs visualised using angiography in the same cohort.60 Utilisation of peak systolic flow is accurate at predicting CMI. A peak systolic flow of >275 cm/s or no flow in the SMA and peak systolic flow of >200 cm/s or no flow in the coeliac artery are indicative of >70% angiographic stenosis of the respective vessels with a high degree of sensitivity and specificity (coeliac artery: sensitivity 87%, specificity 80%; SMA: sensitivity 92%, specificity 96%60; Fig 4).
Median arcuate ligament syndrome can also be evaluated with dynamic duplex imaging; positional changes in peak systolic and diastolic velocities can be identified. With inspiration, the coeliac artery moves inferiorly to a more vertical orientation relieving the compression of the ligamentous band. The syndrome is suggested by a raised peak velocity on expiration. From their small cohort, Gruber et al.61 suggested that maximum expiratory peak velocities above 350 cm/s and an atypical coeliac trunk deflection angle above 50 are the most reliable indicators for median arcuate ligament compression.61 Doppler endoscopic ultrasound has also been used to evaluate CMI, this technique has a lower sensitivity (63% versus 80%) but higher specificity (84% versus 78%) compared with standard transabdominal Doppler ultrasound.62 As in AMI, the reference standard for imaging diagnosis of CMI has been formal angiography. Again for the reasons previously described, this technique has been superseded by CTA, which is now the imaging method of choice.15 Once again, the 3D reformats provide excellent reconstructions of the visceral vasculature, particularly the proximal SMA, where the majority of atherosclerotic lesions will occur. The findings of focal narrowing, post-stenotic dilatation, and a hook-shaped contour of the coeliac artery at CTA in the absence of atherosclerotic plaque support the diagnosis of median arcuate ligament syndrome. It is important to note, however, that this hooked contour is not specific for the syndrome, given that 10e24% of the normal population demonstrate this anatomy.63 MRA has a role to play in the imaging of CMI.24,25,31,64,65 Coeliac and SMA vessels are readily visible on most MRA studies of the abdomen (Fig 5). No direct comparison has been made for the mesenteric vessels between CTA and MRA.24 However, CTA has been proven superior for the evaluation of renal arteries, which are of similar size.66 A recent prospective analysis of 52 patients comparing the grading of mesenteric artery stenosis focusing on the quality of imaging, found that MRA lagged behind CTA with a mean image quality (out of 5) of 3.80.9 compared with 4.40.7.67 Furthermore, the IMA and peripheral splanchnic vessels are better visualised using CTA because of the higher spatial and temporal resolution of this technique.
Treatment of CMI As with AMI, treatment was traditionally surgical. The first open surgical revascularisation for CMI was a thromboendarterectomy of the SMA reported in 1958.68 Nowadays, surgical reconstruction involves endarterectomy, aorto-mesenteric/coeliac bypass grafting, or internal iliacemesenteric bypass with revascularisation of the visceral arteries via Dacron graft bypassing the stenosed/ occluded segments.52,69 This bypass can be performed in an antegrade or retrograde fashion. The main advantage of grafting direct from the supra-coeliac aorta being that this section of the aorta is often not affected by atherosclerosis; drawbacks include the risk of renal ischaemia and haemodynamic instability. Retrograde bypass from the iliac vessels
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Figure 4 (a) A 68-year-old woman with a 15 month history suggestive of mesenteric angina. Doppler ultrasound imaging performed with a 6 MHz curvilinear probe in the sagittal plane demonstrates a tight proximal SMA stenosis (arrow) with significant aliasing of Doppler signal distally (arrowhead). (b) Significantly elevated systolic velocities of >500 cm/s are demonstrated distal to the stenosis. The stenosis was managed with percutaneous stenting. Via a left brachial approach, a 5 F Destination sheath (Terumo, Surrey, UK) was advanced to the SMA origin. (c) A guide wire was advanced across the stenosis and a 6 mm 24 mm balloon mounted stent (arrow) was deployed with good angiographic result.
provides a more direct surgical approach and less haemodynamic instability.53 Angioplasty of the SMA was first reported in 1980.70 Subsequently, there has been a significant shift towards endovascular procedures (Fig 4c). This is due to the decreased peri-operative morbidity and mortality associated with the percutaneous approach.71,72 Significant
Figure 5 (a) MIP reconstructions from a visceral 1.5 T MRA. Coronal imaging demonstrates a tight stenosis of the proximal SMA (arrow), whereas sagittal imaging of the same patient (b) demonstrates tight stenosis of both the proximal coeliac trunk (arrowhead) and SMA (arrow) with obvious post-stenotic dilatation of the coeliac trunk. MRI Images courtesy of Dr Giles Roditi, Consultant Radiologist, Glasgow Royal Infirmary.
debate exists about the most appropriate approach for endovascular treatment in CMI. The number of vessels to treat and covered versus bare metal stents are two of the areas where there has been research focus in the last 5 years. Conflicting evidence exists about the number of vessels to re-vascularise, Malgor et al.73 concluded that dual vessel (coeliac artery and SMA) stenting does not reduce the risk of symptom recurrence when compared with single vessel SMA stenting, whereas Peck et al.74 concluded that twovessel endovascular treatment is protective against symptom recurrence and re-intervention. Single vessel coeliac artery stenting is associated with a higher recurrence rate (38%).73 A cross-site retrospective study comparing the use of bare metal and covered stents in CMI concluded that covered stents were associated with less re-stenosis (534% versus 926%, p¼0.003), symptomatic recurrences (505% versus 924%, p¼0.003), and re-interventions (56e5% versus 916%, p¼0.005) than bare metal stents and also that they had better primary patency at 3 years (926% versus 525%, p<0.003).75 Pecoraro et al.76 recently published a systematic review of all literature to August 2010 comparing endovascular and surgical intervention in CMI. After strict inclusion and exclusion criteria were met, 43 papers were included in the review. In 18 studies patients were treated endovascularly, 16 via surgery, and nine with a mixture of both therapies. In total, 786 patients underwent endovascular treatment compared with open surgery in 1009. Technical success rates of 95.08% and 93.24% were reported with a statistically significant difference found in favour of surgery. Endovascular therapy showed a better 30 day mortality rate (3.56% versus 7.23%, p<0.001) and peri-operative morbidity rate (13.23% versus 33.06%, p<0.001); however, survival data at 1, 2, 3, and 5 years showed no statistically significant difference between the groups. Surgery has better primary (80.93% versus 49.12%) and secondary patency rates (97.93% versus 87.95%). A statistically significant superior number of
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patients faced recurrence of symptoms after endovascular treatment and 18.4% of these went on to have surgery. This particular result may be explained by the number of vessels re-vascularised. A significantly higher number of vessels per patient were re-vascularised surgically than percutaneously (1593 versus 1007).76 Patients with CMI are typically arteriopaths with significant cardiovascular and anaesthetic risk factors. They often have poor baseline nutritional status, which is an independent risk factor for those undergoing gastrointestinal surgery.77,78 These additional factors should be considered when deciding on an appropriate therapeutic strategy. Given the lower peri-operative morbidity and mortality rates associated with percutaneous revascularisation, this approach should be considered as the first-line treatment in most CMI patients especially those suffering with malnutrition. Surgery should be restricted to low-risk patients, those with long life expectancy, or those in whom endovascular treatment is not possible. Endovascular therapy can also be performed as a bridging therapy to surgery if required.76 Endovascular therapies have been described in the management of median arcuate ligament syndrome; however, they fail to protect against the constricting band, which moves during respiration and stent fracture is a risk.55,79 The most reliable treatment, if treatment is deemed necessary, comprises open or laparoscopic surgery with division of the median arcuate ligament, removal of the coeliac ganglion, and coeliac artery reconstruction if required.54
Conclusion As radiologists AMI and CMI are conditions that must be considered in the differential diagnosis of abdominal pain, particularly in the arteriopath. Currently, mesenteric ischaemia is best evaluated using CTA. This technique enables interrogation of both the vascular tree and the ancillary intra-abdominal findings. Research and development within our specialty may lead to more widespread clinical use of MRI and PET imaging techniques. Percutaneous endovascular intervention has become the first-line treatment approach for CMI and is being increasingly used in early presentation AMI.
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7. Greene FL, Ariyan S, Stansel Jr HC. Mesenteric and peripheral vascular ischemia secondary to ergotism. Surgery 1977 Feb;81:176e9. 8. Patel T, Kuladhipati I, Shah S. Successful percutaneous endovascular management of acute post-traumatic superior mesenteric artery dissection using a transradial approach. J Invasive Cardiol 2010;22:E61e4. € rck M. D-dimer testing in patients with sus9. Acosta S, Nilsson TK, Bjo pected acute thromboembolic occlusion of the superior mesenteric artery. Br J Surg 2004 Aug;91:991e4. 10. Murray MJ, Gonze MD, Nowak LR, et al. Serum D-lactate levels as an aid to diagnosing acute intestinal ischemia. Am J Surg 1994 Jun;167:575e8. € rck M. Acute thrombo-embolic occlusion of the superior 11. Acosta S, Bjo mesenteric artery: a prospective study in a well-defined population. Eur J Vasc Endovasc Surg Off J Eur Soc Vasc Surg 2003 Aug;26:179e83. 12. Evennett NJ, Petrov MS, Mittal A, et al. Systematic review and pooled estimates for the diagnostic accuracy of serological markers for intestinal ischemia. World J Surg 2009;33:1374e83. 13. Guzel M, Sozuer EM, Salt O, et al. The value of the serum I-FABP level for diagnosing acute mesenteric ischaemia. Surg Today 2014;44:2072e6. 14. Matsumoto S, Seikine K, Funaoka H, et al. Diagnostic performance of plasma biomarkers in patients with acute intestinal ischaemia. Br J Surg 2014;101:232e8. 15. Oliva IB, Davarpanah AH, Rybicki FJ, et al. ACR appropriateness criteria imaging of mesenteric ischemia. Abdom Imaging 2013;38:714e9. 16. Clark RA, Gallant TE. Acute mesenteric ischemia: angiographic spectrum. AJR Am J Roentgenol 1984;142:555e62. 17. Oldenburg WA, Lau LL, Rodenberg TJ, et al. Acute mesenteric ischemia: a clinical review. Arch Intern Med 2004;164:1054e62. 18. Wolf EL, Sprayregen S, Bakal CW. Radiology in intestinal ischemia. Plain film, contrast, and other imaging studies. Surg Clin North Am 1992;72:107e24. 19. Reginelli A, Genovese E, Cappabianca S, et al. Intestinal ischemia: US-CT findings correlations. Crit Ultrasound J 2013;5(Suppl. 1):S7. 20. Horton KM, Fishman EK. Multi-detector row CT of mesenteric ischemia: can it be done? Radiogr Rev Publ Radiol Soc North Am Inc 2001;21:1463e73. 21. Kirkpatrick IDC, Kroeker MA, Greenberg HM. Biphasic CT with mesenteric CT angiography in the evaluation of acute mesenteric ischemia: initial experience. Radiology 2003;229:91e8. 22. Chou CK. CT manifestations of bowel ischemia. AJR Am J Roentgenol 2002;178:87e91. 23. Aschoff AJ, Stuber G, Becker BW, et al. Evaluation of acute mesenteric ischemia: accuracy of biphasic mesenteric multi-detector CT angiography. Abdom Imaging 2009;34:345e57. 24. Shih M-CP, Hagspiel KD. CTA and MRA in mesenteric ischemia: part 1. Role in diagnosis and differential diagnosis. AJR Am J Roentgenol 2007;188:452e61. 25. Shih M-CP, Angle JF, Leung DA, et al. CTA and MRA in mesenteric ischemia: part 2. Normal findings and complications after surgical and endovascular treatment. AJR Am J Roentgenol 2007;188:462e71. 26. Ofer A, Abadi S, Nitecki S, et al. Multidetector CT angiography in the evaluation of acute mesenteric ischemia. Eur Radiol 2009;19:24e30. 27. Taourel PG, Deneuville M, Pradel JA, et al. Acute mesenteric ischemia: diagnosis with contrast-enhanced CT. Radiology 1996;199:632e6. 28. Furukawa A, Kanasaki S, Kono N, et al. CT diagnosis of acute mesenteric ischaemia from various causes. AJR Am J Roentgenol 2009;192:408e16. 29. Duron VP, Rutigliano S, Machan JT, et al. Computed tomographic diagnosis of pneumatosis intestinalis: clinical measures predictive of the need for surgical intervention. Arch Surg 2011;146:506e10. a SM, et al. Distinguishing benign and life30. Lee KS, Hwang S, Hurtado Ru threatening pneumatosis intestinalis in patients with cancer by CT imaging features. AJR Am J Roentgenol 2013;200:1042e7. 31. Meaney JF, Prince MR, Nostrant TT, et al. Gadolinium-enhanced MR angiography of visceral arteries in patients with suspected chronic mesenteric ischemia. J Magn Reson Imaging 1997;7:171e6. 32. Meaney JF. Non-invasive evaluation of the visceral arteries with magnetic resonance angiography. Eur Radiol 1999;9:1267e76. 33. Somma F, Berritto D, Iacobellis F, et al. 7T mMRI of mesenteric venous ischemia in a rat model: timing of the appearance of findings. Magn Reson Imaging 2013;31:408e13.
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Review
Radiology and mesenteric ischaemia E. McCarthy, M. Little, J. Briggs, J. Sutcliffe, C.R. Tapping, R. Patel, M.J. Bratby, R. Uberoi* Oxford University Hospitals, Department of Radiology, John Radcliffe Hospital, Headley Way, Headington, Oxford, OX3 9DU, UK
article in formation Article history: Received 18 December 2013 Received in revised form 29 October 2014 Accepted 17 February 2015
This review focuses on the radiology of mesenteric ischaemia. Covering the acute and chronic presentations, both of which result from impaired vascularisation of the gastrointestinal tract, we evaluate the role of radiographs, ultrasound, CT, MRI, and catheter angiography in the diagnosis of these conditions. Looking to the future, we also assess some of the emerging imaging techniques. Across medicine and surgery there has been a significant shift towards minimally invasive interventions. Although percutaneous revascularisation of chronic mesenteric ischaemia has been performed for some time, there has been a developing trend for the use of such techniques in acute mesenteric ischaemia. We evaluate the available evidence for the use of these percutaneous interventions and assess how they compare with or in some instances compliment traditional surgical alternatives. Ó 2015 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
Introduction
AMI
Mesenteric ischaemia encompasses both acute and chronic conditions resulting from impaired blood flow to the intestines. Acute mesenteric ischaemia (AMI) is a lifethreatening event that requires prompt identification and treatment. Chronic mesenteric ischaemia (CMI) is a more insidious entity, often a diagnosis of exclusion, presenting with progressive cachexia and reproducible post-prandial pain. In this review, we focus on the radiological investigations being employed in current clinical practice and those in evolution. We also evaluate the role of imageguided interventions and how they compare with and compliment the surgical alternatives.
AMI is a rare but life-threatening condition requiring prompt identification and treatment. AMI has a mortality ranging between 30 and 90% dependent on aetiology and time to intervention.1 Time at presentation is a crucial factor. Animal studies carried out by Udassin et al.2 demonstrated the effects of absolute ischaemia on the mucosal lining of the small intestine. Structural changes of the villi were identified at 15 minutes with trans-mural necrosis and gangrene identified at 6 hours2. The aetiology of AMI can be divided into occlusive, and non-occlusive causes (Table 1). Occlusive disease accounts for 85% of presentations: in situ arterial thrombosis in 50%, including dissection (Fig 1); embolic thrombus in approximately 20%; and mesenteric venous thrombosis in 15%.3 Atherosclerotic plaque has a predilection for the vessel ostiae with ulceration of these plaques leading to thrombosis. Although atherosclerotic plaque does not demonstrate predilection for any particular vascular territory, 50%
* Guarantor and correspondent: R. Uberoi, Oxford University Hospitals, Department of Radiology, John Radcliffe Hospital, Headley Way, Headington, Oxford, OX3 9DU, UK. Tel.: þ44 (0) 01865 741166; fax: þ44 (0) 01865 220801. E-mail address: [email protected] (R. Uberoi).
http://dx.doi.org/10.1016/j.crad.2015.02.012 0009-9260/Ó 2015 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
E. McCarthy et al. / Clinical Radiology 70 (2015) 698e705
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Table 1 Causes of acute mesenteric ischaemia. Occlusive
Non-occlusive
Arterial occlusion
Hypovolaemia
Thromboembolic disease Dissection Venous thrombosis
Cardiogenic/hypovolaemic shock Transection Vasoconstriction
Hyper-coagulable state Recent surgery Abdominal sepsis Portal hypertension Mechanical compression
Ergot alkaloids Cocaine Vasculitides
of occlusive arterial embolic episodes involve the superior mesenteric artery (SMA; Fig 2). The origin of this vessel usually has a less acute angle than the coeliac artery making it a more likely destination for emboli. Emboli usually lodge distal to the middle colic and jejunal SMA branches with a small proportion lodging proximally at the vessel origin. 20% of patients with SMA emboli will have synchronous embolisation of another arterial bed.4,5 Symptomatic inferior mesenteric artery (IMA) emboli are less frequent given the smaller vessel calibre and the extensive collateralisation from SMA, and middle and inferior haemorrhoidal territories. Non-occlusive causes of AMI account for 15% and are the result of low flow states, such as cardiogenic shock, ergot medications, and trauma.3,6e8 Patients typically present with abdominal pain, nausea, vomiting, and less frequently, bloody diarrhoea. They are likely to have raised C-reactive protein, leukocytosis, metabolic acidosis, elevated D-dimers, can be Figure 2 (a) Axial section from an arterial-phase CT examination demonstrating luminal filling defect in the SMA of a 66-year-old woman who presented with abdominal pain (arrow). No associated bowel wall abnormalities were identified. Features were consistent with acute embolic mesenteric ischaemia. (b) Formal catheter angiography demonstrating a filling defect in the distal main SMA (arrow). (c) This was treated via thrombo-aspiration through a 6 F guide catheter with good angiographic result (arrow).
Figure 1 Type A dissection flap extending into the SMA (arrow) of a 71-year-old man. This flap resulted in thrombosis of a short segment of the proximal SMA. The patient underwent emergent aortic root repair. Despite the SMA dissection flap being documented, the short segment thrombosis was not initially identified leading to small bowel ischaemia in the early postoperative period.
hyperkalaemic, and have a raised lactate.9 Raised lactate is a late finding, associated with concomitant intestinal necrosis and a poor outcome, (sensitivity 90e96%, specificity 60e87%).10 Indeed, although classic descriptions include metabolic acidosis, one prospective clinical trial described a metabolic alkalosis being more common secondary to the profound vomiting associated with this condition.11 Recent clinical reviews have focused on biomarkers for the earlier clinical detection of intestinal ischaemia. These include intestinal fatty acid binding protein (I-FABP) and alphaglutathione S transferase (GST).12e14
Imaging of AMI A variety of imaging techniques have been employed in the evaluation of AMI. Radiography, duplex ultrasound, multi-
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section CT, endoscopy, MRI, and angiography have all been evaluated. Angiography has historically been the reference standard for the diagnosis of AMI, and its introduction initially led to improved diagnosis with better survival rates.15,16 Angiography allows both diagnosis and the potential to carry out therapeutic procedures simultaneously. However, this is not available in all units, is an invasive procedure, and is uncommonly performed in the acute setting. Erect chest radiography and/or plain films of the abdomen are frequently obtained in patients with abdominal pain. Their role in the evaluation of AMI is limited; an abdominal radiograph cannot exclude AMI as 25% of patients with the condition will have a normal abdominal film.17 Bowel obstruction, bowel wall oedema, intraperitoneal free gas, portal venous gas, and pneumatosis intestinalis can be identified at radiography; however, these findings are typically identified late, often when bowel ischaemia/infarction has already developed.18 Ultrasound assessment is usually carried out with lowfrequency curvilinear probes. The coeliac artery and SMA are identified coming off the aorta in the sagittal plane. The IMA is often difficult to visualise. The vessels are interrogated using Doppler mode, which is highly specific (92e100%) but has a lower sensitivity (70e89%) for identifying vascular occlusions. It is less successful in the assessment of non-occlusive thrombus or distal occlusion.15 In the early phase of arterial occlusive AMI, ultrasound may demonstrate SMA occlusion and bowel spasm. In the intermediate phase, ultrasound is less informative due to gaseous accumulation in the bowel with resultant acoustic impedance. Later, fluid-filled loops, decreased or absent peristalsis, bowel wall thinning, or peritoneal free fluid may be seen. In venous occlusive AMI, ultrasound may reveal focal SMV or portal thrombus, decreased peristalsis, increased intraluminal secretions, and segmental mural thickening.19 In advanced cases, intramural gas and portal venous gas may be evident. This technique is helpful in narrowing the differential causes of abdominal pain but actual image quality and reproducibility of results is operator dependent, and in certain instances, can be limited by overlying bowel gas. CT angiography (CTA) has evolved over the past decade and is currently recommended as the first-line imaging technique.15,20 CTA, unlike angiography is widely available and non-invasive. In our institution CTA is performed using a 64 section system (Lightspeed, GE Healthcare, Bucks, UK). The imaging parameters are 0.625 mm collimation, 0.5 pitch, 0.4 seconds rotation speed, 120 kVp, smart tube current, and a soft reconstruction kernel. We use 100 ml iopamidol (370 mg iodine/ml; Niopam 370, Bracco UK, Bucks, UK). Imaging is obtained at 30 seconds with contrast medium administered at a rate of 3 ml/s. Evolution of multi-section CT technology allows the reconstruction of vessels in three-dimensional (3D) planes. Added to that, CT affords the ability to image the gastrointestinal tract for the ancillary findings of AMI. It also allows evaluation of the genitourinary tract for differential diagnoses in the acute abdomen. Many studies document the success of CT in identifying findings suggestive of AMI.19e26
Signs associated with AMI include vascular luminal filling defects or truncation of the vessels, focal lack of mural enhancement, bowel wall thickening, fat stranding, pneumatosis intestinalis, portal venous gas (Fig 3), intraperitoneal free gas, and ascites. Bowel wall thickening is the most frequently observed finding in AMI. It has a high sensitivity (85e88%) but as expected is much less specific (61e72%). Intra-luminal defects or occlusions of the mesenteric vessels are less sensitive (12e15%) but are again highly specific (94e100%). A combination of signs will help increase reader confidence. Combining bowel wall abnormalities (thickening/lack of mural enhancement) with pneumatosis intestinalis increases specificity to between 97 and 100%.22,23,26,27 Paradoxically, hyper-enhancement of the bowel wall can also be an indicator of acute ischaemia. This may be secondary to hyperaemia (from mesenteric venous occlusion or from reperfusion injury.28 Interpretation of pneumatosis intestinalis can be challenging for the reporting radiologist. Pneumatosis intestinalis refers to gas within the wall of the bowel, and a good rule of thumb is to look for intramural gas in the dependent colon. The importance of isolated pneumatosis intestinalis is controversial. Duron et al.29 evaluated a large group of patients with pneumatosis using CT, 47% of their cohort with this finding improved or had negative laparotomies. Lee et al.30 investigated an oncological cohort and found that in patients with cancer, benign pneumatosis (requiring no intervention, that resolved or improved on subsequent imaging) was confined to the colon, whereas clinically worrisome pneumatosis (destined for laparotomy), although being associated with bowel dilatation, stranding, mural thickening, and ascites, was also more likely to be limited to the small bowel. These studies reiterate the importance of considering all imaging findings and the clinical context when considering a diagnosis of AMI. Furthermore, it is important to be able to distinguish benign variants of pneumatosis intestinalis, in particular pneumatosis cystoides intestinalis. The cystoides variant typically presents with sub-mucosal/sub-serosal cyst formation and although
Figure 3 Axial section on lung windows through the abdomen of a 69-year-old woman. Pneumatosis intestinalis (arrow) and gas within an SMV tributary (arrowhead) are demonstrated, features consistent with ischaemic bowel.
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this can also result in pneumoperitoneum, it tends to have a more benign presentation and clinical course. Pneumatosis cystoides is associated with connective tissue disorders, chronic obstructive airways disease, and steroid use. Magnetic resonance angiography (MRA) at 1.5 T has a high sensitivity and specificity for evaluation of occlusions or high-grade stenoses of the proximal coeliac trunk or SMA. It has limited value in the evaluation of distal mesenteric occlusions.31,32 MRA is time consuming and not as freely available as CT, which limits its usefulness in the acute setting. Recent lab based research has examined the possible role of 3 T, 7 T MRI, and positron-emission tomography (PET) in the evaluation of AMI.33e37 Macroscopic, 7 T MRI and histological appearances after ligation of rodent IMA, SMA, and SMV have been evaluated with an encouraging positive correlation between the imaging and histological findings. Abnormalities were identified on imaging as early as 30 minutes post-ligation, progressively worsening until the end point at 8 hours. MRI has the potential to become the imaging method of choice in the future with further technological evolution. Similarly, PET has been able to demonstrate significant reductions in porcine hepatic perfusion (40%), intrahepatic blood content (75%), and portal blood flow (45%) after induced intestinal ischaemia. This reduction in flow and blood content persisted during reperfusion of the intestine.37 Further studies will be required to assess the possible clinical role of PET in AMI imaging.
Image-guided management of AMI Treatment of AMI traditionally involved laparotomy and segmental bowel resection with mesenteric revascularisation via surgical bypass if required. Minimally invasive radiologically guided interventions have been described and can be attempted in the absence of peritonism or imaging findings consistent with perforation. Therapeutic endovascular options include aspiration thromboembolectomy, pharmacological and/or mechanical thrombolysis, antegrade visceral arterial stenting, and hybrid intra-operative retrograde stenting. Percutaneous access is usually obtained via the femoral or brachial artery. Historical data demonstrate higher survival rates when vasodilators have been administered as part of the treatment of AMI.38 To this effect transcatheter papaverine can be used in acute arterial occlusion and in non-occlusive vasospastic AMI. Papaverine is a phosphodiesterase inhibitor that increases circulating intracellular levels of cyclic adenosine monophosphate (cAMP), a vascular smooth muscle relaxant. Papaverine is administered as a bolus dose of 60 mg followed by an infusion (30e60 mg/h) continued for 24e48 hours with repeat angiograms performed every 24 hours. A stable catheter position is required to avoid intra-aortic delivery, which would result in profound hypotension.16,38,39 However, there has been no significant addition to the evidence basis for this therapy over the course of the last 30 years. Catheter thrombo-aspiration is a well-documented approach.40,41 This is usually performed with a long
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arterial sheath placed as close to the luminal obstruction as possible. A wide-bore guide catheter (6e8 F) is repeatedly manoeuvred through the thrombus/embolus while back suction is placed on the catheter using a 20 ml syringe. A number of attempts are usually required to dislodge the obstruction (Fig 2bec). Intra-arterial thrombolytic therapies including streptokinase, urokinase, and tissue plasminogen activator (t-PA) have been described. In one systematic review, 30 of 48 (63%) patients avoided surgery after primary treatment with thrombolytics.42 Intra-arterial thrombolysis has not become a favoured monotherapy due to the time taken to re-vascularise and the potential bleeding risk from the ischaemic mucosa. In clinical practice, a combination of approaches may be required for re-vascularisation; this is where intra-arterial thrombolysis can be quite useful in the treatment of residual clot.43 Recently, the successful use of mechanical and aspirational thrombectomy devices including Aspirex S (Straub Medical, Switzerland), Rotarex S (Straub Medical, Switzerland), Angiojet (Bayer, CA, USA), and Merci Retriever (Concentric Medical, The Netherlands) have been described, all be it in small case series and case reports.44e46 Once the acute luminal obstruction has been treated, there is often an underlying stenosis that needs to be managed, and this can be carried out during the same procedure. Percutaneous transluminal angioplasty of the SMA in AMI has a poor long-term outcome and arterial dissection as a result of angioplasty would render subsequent stenting difficult.45 As such, primary stenting for critically narrowed lesions is the approach of choice. The use of both balloon mounted and self-expanding stents have been described. The more precise balloon mounted approach appears favourable for proximal lesions, whereas the self-expanding stents accommodate distal SMA tortuosity better.47 Seven to 9 mm diameter stents are commonly deployed in the coeliac artery and SMA. Intra-operative retrograde transluminal angioplasty and stenting of the SMA has also been successful. This approach combines endovascular techniques and surgery, allowing assessment and resection of the nonviable bowel.48,49 At the time of laparotomy, an arteriotomy is made in the main trunk of the SMA and a wire is passed retrogradely into the aorta. This is then snared in the aorta via a femoral (or brachial) approach and the wire pulled through. If required, a surgical embolectomy balloon can be passed through the occlusion and the vessel can then be stented. A small retrospective study of 13 patients demonstrated lower in-hospital mortality rates associated with this hybrid approach (17%) compared with surgical bypass (80%) and percutaneous stenting at 100%.49 A recent evidence-based review concludes that postoperative complications and inpatient mortality rates are lower for endovascular therapies than for open surgery and that endovascular thrombolysis prior to open surgery may reduce the length of bowel resected. The evidence is limited and management should be decided on a case-bycase basis.50
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CMI The condition usually occurs in patients over 60 and demonstrates a 3:1 female predominance.51 This is despite the fact that up to 60% of the normal population demonstrate some degree of mesenteric arterial stenosis.52 Patients classically present with epigastric/periumbilical postprandial pain. This pain typically commences 30 minutes post-eating, lasts 1e2 hours and may result in sitophobia (fear of food) with significant consequent weight loss. Traditional descriptions require occlusion or high-grade stenosis of two of the three visceral arteries.53 This is because of the protection provided by presence of a number of collateral pathways within the mesenteric circulation including the pancreatico-duodenal arcade, marginal artery of Drummond, arc of Barkow, arc of Riolan and the arc of Buhler. In CMI, the SMA is the most frequently involved vessel. Isolated stenosis of the SMA resulting in symptoms has been reported.54 Isolated cases of coeliac artery involvement have also been described; however, this is more likely to be the result of median arcuate ligament syndrome. This syndrome typically presents with similar symptoms to CMI, although in a younger population. Median arcuate ligament syndrome occurs due to compression of the coeliac artery and coeliac ganglia by the median arcuate ligament, a fibrous arch formed by the right and left diaphragmatic crura.55 Atherosclerosis is the cause of CMI in the vast majority of cases. Less commonly CMI can be attributed to fibromuscular dysplasia or arcuate ligament syndrome. Rarer causes include; polyarteritis nodosa, Buerger’s disease, Takayasu’s disease, arterial dissection, and abdominal aortic aneurysm.56e58
Imaging of CMI Radiographs have no role to play in the diagnosis of CMI as patients have not developed bowel necrosis, and therefore, the radiograph will likely be normal or demonstrate non-specific findings.15 Unlike in the acute setting, Doppler ultrasound has been more successfully employed in the chronic presentation. This imaging technique has the added benefit of dynamic assessment of flow through anatomically narrowed vessel segments. Duplex is best performed in the fasting state and early in the day to avoid bowel gas.59 Anecdotally the weight loss, which invariably accompanies this condition, should aid sonography, although vessels may remain difficult to visualise. In one study, 83% of coeliac trunks and 93% of SMA vessels were visualised on the initial duplex studies compared with 100% of coeliac trunks and 99% of SMAs visualised using angiography in the same cohort.60 Utilisation of peak systolic flow is accurate at predicting CMI. A peak systolic flow of >275 cm/s or no flow in the SMA and peak systolic flow of >200 cm/s or no flow in the coeliac artery are indicative of >70% angiographic stenosis of the respective vessels with a high degree of sensitivity and specificity (coeliac artery: sensitivity 87%, specificity 80%; SMA: sensitivity 92%, specificity 96%60; Fig 4).
Median arcuate ligament syndrome can also be evaluated with dynamic duplex imaging; positional changes in peak systolic and diastolic velocities can be identified. With inspiration, the coeliac artery moves inferiorly to a more vertical orientation relieving the compression of the ligamentous band. The syndrome is suggested by a raised peak velocity on expiration. From their small cohort, Gruber et al.61 suggested that maximum expiratory peak velocities above 350 cm/s and an atypical coeliac trunk deflection angle above 50 are the most reliable indicators for median arcuate ligament compression.61 Doppler endoscopic ultrasound has also been used to evaluate CMI, this technique has a lower sensitivity (63% versus 80%) but higher specificity (84% versus 78%) compared with standard transabdominal Doppler ultrasound.62 As in AMI, the reference standard for imaging diagnosis of CMI has been formal angiography. Again for the reasons previously described, this technique has been superseded by CTA, which is now the imaging method of choice.15 Once again, the 3D reformats provide excellent reconstructions of the visceral vasculature, particularly the proximal SMA, where the majority of atherosclerotic lesions will occur. The findings of focal narrowing, post-stenotic dilatation, and a hook-shaped contour of the coeliac artery at CTA in the absence of atherosclerotic plaque support the diagnosis of median arcuate ligament syndrome. It is important to note, however, that this hooked contour is not specific for the syndrome, given that 10e24% of the normal population demonstrate this anatomy.63 MRA has a role to play in the imaging of CMI.24,25,31,64,65 Coeliac and SMA vessels are readily visible on most MRA studies of the abdomen (Fig 5). No direct comparison has been made for the mesenteric vessels between CTA and MRA.24 However, CTA has been proven superior for the evaluation of renal arteries, which are of similar size.66 A recent prospective analysis of 52 patients comparing the grading of mesenteric artery stenosis focusing on the quality of imaging, found that MRA lagged behind CTA with a mean image quality (out of 5) of 3.80.9 compared with 4.40.7.67 Furthermore, the IMA and peripheral splanchnic vessels are better visualised using CTA because of the higher spatial and temporal resolution of this technique.
Treatment of CMI As with AMI, treatment was traditionally surgical. The first open surgical revascularisation for CMI was a thromboendarterectomy of the SMA reported in 1958.68 Nowadays, surgical reconstruction involves endarterectomy, aorto-mesenteric/coeliac bypass grafting, or internal iliacemesenteric bypass with revascularisation of the visceral arteries via Dacron graft bypassing the stenosed/ occluded segments.52,69 This bypass can be performed in an antegrade or retrograde fashion. The main advantage of grafting direct from the supra-coeliac aorta being that this section of the aorta is often not affected by atherosclerosis; drawbacks include the risk of renal ischaemia and haemodynamic instability. Retrograde bypass from the iliac vessels
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Figure 4 (a) A 68-year-old woman with a 15 month history suggestive of mesenteric angina. Doppler ultrasound imaging performed with a 6 MHz curvilinear probe in the sagittal plane demonstrates a tight proximal SMA stenosis (arrow) with significant aliasing of Doppler signal distally (arrowhead). (b) Significantly elevated systolic velocities of >500 cm/s are demonstrated distal to the stenosis. The stenosis was managed with percutaneous stenting. Via a left brachial approach, a 5 F Destination sheath (Terumo, Surrey, UK) was advanced to the SMA origin. (c) A guide wire was advanced across the stenosis and a 6 mm 24 mm balloon mounted stent (arrow) was deployed with good angiographic result.
provides a more direct surgical approach and less haemodynamic instability.53 Angioplasty of the SMA was first reported in 1980.70 Subsequently, there has been a significant shift towards endovascular procedures (Fig 4c). This is due to the decreased peri-operative morbidity and mortality associated with the percutaneous approach.71,72 Significant
Figure 5 (a) MIP reconstructions from a visceral 1.5 T MRA. Coronal imaging demonstrates a tight stenosis of the proximal SMA (arrow), whereas sagittal imaging of the same patient (b) demonstrates tight stenosis of both the proximal coeliac trunk (arrowhead) and SMA (arrow) with obvious post-stenotic dilatation of the coeliac trunk. MRI Images courtesy of Dr Giles Roditi, Consultant Radiologist, Glasgow Royal Infirmary.
debate exists about the most appropriate approach for endovascular treatment in CMI. The number of vessels to treat and covered versus bare metal stents are two of the areas where there has been research focus in the last 5 years. Conflicting evidence exists about the number of vessels to re-vascularise, Malgor et al.73 concluded that dual vessel (coeliac artery and SMA) stenting does not reduce the risk of symptom recurrence when compared with single vessel SMA stenting, whereas Peck et al.74 concluded that twovessel endovascular treatment is protective against symptom recurrence and re-intervention. Single vessel coeliac artery stenting is associated with a higher recurrence rate (38%).73 A cross-site retrospective study comparing the use of bare metal and covered stents in CMI concluded that covered stents were associated with less re-stenosis (534% versus 926%, p¼0.003), symptomatic recurrences (505% versus 924%, p¼0.003), and re-interventions (56e5% versus 916%, p¼0.005) than bare metal stents and also that they had better primary patency at 3 years (926% versus 525%, p<0.003).75 Pecoraro et al.76 recently published a systematic review of all literature to August 2010 comparing endovascular and surgical intervention in CMI. After strict inclusion and exclusion criteria were met, 43 papers were included in the review. In 18 studies patients were treated endovascularly, 16 via surgery, and nine with a mixture of both therapies. In total, 786 patients underwent endovascular treatment compared with open surgery in 1009. Technical success rates of 95.08% and 93.24% were reported with a statistically significant difference found in favour of surgery. Endovascular therapy showed a better 30 day mortality rate (3.56% versus 7.23%, p<0.001) and peri-operative morbidity rate (13.23% versus 33.06%, p<0.001); however, survival data at 1, 2, 3, and 5 years showed no statistically significant difference between the groups. Surgery has better primary (80.93% versus 49.12%) and secondary patency rates (97.93% versus 87.95%). A statistically significant superior number of
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patients faced recurrence of symptoms after endovascular treatment and 18.4% of these went on to have surgery. This particular result may be explained by the number of vessels re-vascularised. A significantly higher number of vessels per patient were re-vascularised surgically than percutaneously (1593 versus 1007).76 Patients with CMI are typically arteriopaths with significant cardiovascular and anaesthetic risk factors. They often have poor baseline nutritional status, which is an independent risk factor for those undergoing gastrointestinal surgery.77,78 These additional factors should be considered when deciding on an appropriate therapeutic strategy. Given the lower peri-operative morbidity and mortality rates associated with percutaneous revascularisation, this approach should be considered as the first-line treatment in most CMI patients especially those suffering with malnutrition. Surgery should be restricted to low-risk patients, those with long life expectancy, or those in whom endovascular treatment is not possible. Endovascular therapy can also be performed as a bridging therapy to surgery if required.76 Endovascular therapies have been described in the management of median arcuate ligament syndrome; however, they fail to protect against the constricting band, which moves during respiration and stent fracture is a risk.55,79 The most reliable treatment, if treatment is deemed necessary, comprises open or laparoscopic surgery with division of the median arcuate ligament, removal of the coeliac ganglion, and coeliac artery reconstruction if required.54
Conclusion As radiologists AMI and CMI are conditions that must be considered in the differential diagnosis of abdominal pain, particularly in the arteriopath. Currently, mesenteric ischaemia is best evaluated using CTA. This technique enables interrogation of both the vascular tree and the ancillary intra-abdominal findings. Research and development within our specialty may lead to more widespread clinical use of MRI and PET imaging techniques. Percutaneous endovascular intervention has become the first-line treatment approach for CMI and is being increasingly used in early presentation AMI.
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