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Editor's Choice – Management of the Diseases of Mesenteric Arteries and Veins

Clinical Practice Guidelines of the European Society of Vascular Surgery (ESVS)
  • Author Footnotes
    a Writing Committee: M. Björck∗ (Chair) (Sweden), M. Koelemay (Co-chair) (The Netherlands), S. Acosta (Sweden), F. Bastos Goncalves (Portugal), T. Kölbel (Germany), J.J. Kolkman (The Netherlands), T. Lees (UK), J.H. Lefevre (France), G. Menyhei (Hungary), G. Oderich (USA).
    M. Björck
    Footnotes
    a Writing Committee: M. Björck∗ (Chair) (Sweden), M. Koelemay (Co-chair) (The Netherlands), S. Acosta (Sweden), F. Bastos Goncalves (Portugal), T. Kölbel (Germany), J.J. Kolkman (The Netherlands), T. Lees (UK), J.H. Lefevre (France), G. Menyhei (Hungary), G. Oderich (USA).
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  • Author Footnotes
    a Writing Committee: M. Björck∗ (Chair) (Sweden), M. Koelemay (Co-chair) (The Netherlands), S. Acosta (Sweden), F. Bastos Goncalves (Portugal), T. Kölbel (Germany), J.J. Kolkman (The Netherlands), T. Lees (UK), J.H. Lefevre (France), G. Menyhei (Hungary), G. Oderich (USA).
    M. Koelemay
    Footnotes
    a Writing Committee: M. Björck∗ (Chair) (Sweden), M. Koelemay (Co-chair) (The Netherlands), S. Acosta (Sweden), F. Bastos Goncalves (Portugal), T. Kölbel (Germany), J.J. Kolkman (The Netherlands), T. Lees (UK), J.H. Lefevre (France), G. Menyhei (Hungary), G. Oderich (USA).
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  • Author Footnotes
    a Writing Committee: M. Björck∗ (Chair) (Sweden), M. Koelemay (Co-chair) (The Netherlands), S. Acosta (Sweden), F. Bastos Goncalves (Portugal), T. Kölbel (Germany), J.J. Kolkman (The Netherlands), T. Lees (UK), J.H. Lefevre (France), G. Menyhei (Hungary), G. Oderich (USA).
    S. Acosta
    Footnotes
    a Writing Committee: M. Björck∗ (Chair) (Sweden), M. Koelemay (Co-chair) (The Netherlands), S. Acosta (Sweden), F. Bastos Goncalves (Portugal), T. Kölbel (Germany), J.J. Kolkman (The Netherlands), T. Lees (UK), J.H. Lefevre (France), G. Menyhei (Hungary), G. Oderich (USA).
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  • Author Footnotes
    a Writing Committee: M. Björck∗ (Chair) (Sweden), M. Koelemay (Co-chair) (The Netherlands), S. Acosta (Sweden), F. Bastos Goncalves (Portugal), T. Kölbel (Germany), J.J. Kolkman (The Netherlands), T. Lees (UK), J.H. Lefevre (France), G. Menyhei (Hungary), G. Oderich (USA).
    F. Bastos Goncalves
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    a Writing Committee: M. Björck∗ (Chair) (Sweden), M. Koelemay (Co-chair) (The Netherlands), S. Acosta (Sweden), F. Bastos Goncalves (Portugal), T. Kölbel (Germany), J.J. Kolkman (The Netherlands), T. Lees (UK), J.H. Lefevre (France), G. Menyhei (Hungary), G. Oderich (USA).
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  • Author Footnotes
    a Writing Committee: M. Björck∗ (Chair) (Sweden), M. Koelemay (Co-chair) (The Netherlands), S. Acosta (Sweden), F. Bastos Goncalves (Portugal), T. Kölbel (Germany), J.J. Kolkman (The Netherlands), T. Lees (UK), J.H. Lefevre (France), G. Menyhei (Hungary), G. Oderich (USA).
    T. Kölbel
    Footnotes
    a Writing Committee: M. Björck∗ (Chair) (Sweden), M. Koelemay (Co-chair) (The Netherlands), S. Acosta (Sweden), F. Bastos Goncalves (Portugal), T. Kölbel (Germany), J.J. Kolkman (The Netherlands), T. Lees (UK), J.H. Lefevre (France), G. Menyhei (Hungary), G. Oderich (USA).
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  • Author Footnotes
    a Writing Committee: M. Björck∗ (Chair) (Sweden), M. Koelemay (Co-chair) (The Netherlands), S. Acosta (Sweden), F. Bastos Goncalves (Portugal), T. Kölbel (Germany), J.J. Kolkman (The Netherlands), T. Lees (UK), J.H. Lefevre (France), G. Menyhei (Hungary), G. Oderich (USA).
    J.J. Kolkman
    Footnotes
    a Writing Committee: M. Björck∗ (Chair) (Sweden), M. Koelemay (Co-chair) (The Netherlands), S. Acosta (Sweden), F. Bastos Goncalves (Portugal), T. Kölbel (Germany), J.J. Kolkman (The Netherlands), T. Lees (UK), J.H. Lefevre (France), G. Menyhei (Hungary), G. Oderich (USA).
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    a Writing Committee: M. Björck∗ (Chair) (Sweden), M. Koelemay (Co-chair) (The Netherlands), S. Acosta (Sweden), F. Bastos Goncalves (Portugal), T. Kölbel (Germany), J.J. Kolkman (The Netherlands), T. Lees (UK), J.H. Lefevre (France), G. Menyhei (Hungary), G. Oderich (USA).
    T. Lees
    Footnotes
    a Writing Committee: M. Björck∗ (Chair) (Sweden), M. Koelemay (Co-chair) (The Netherlands), S. Acosta (Sweden), F. Bastos Goncalves (Portugal), T. Kölbel (Germany), J.J. Kolkman (The Netherlands), T. Lees (UK), J.H. Lefevre (France), G. Menyhei (Hungary), G. Oderich (USA).
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  • Author Footnotes
    a Writing Committee: M. Björck∗ (Chair) (Sweden), M. Koelemay (Co-chair) (The Netherlands), S. Acosta (Sweden), F. Bastos Goncalves (Portugal), T. Kölbel (Germany), J.J. Kolkman (The Netherlands), T. Lees (UK), J.H. Lefevre (France), G. Menyhei (Hungary), G. Oderich (USA).
    J.H. Lefevre
    Footnotes
    a Writing Committee: M. Björck∗ (Chair) (Sweden), M. Koelemay (Co-chair) (The Netherlands), S. Acosta (Sweden), F. Bastos Goncalves (Portugal), T. Kölbel (Germany), J.J. Kolkman (The Netherlands), T. Lees (UK), J.H. Lefevre (France), G. Menyhei (Hungary), G. Oderich (USA).
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  • Author Footnotes
    a Writing Committee: M. Björck∗ (Chair) (Sweden), M. Koelemay (Co-chair) (The Netherlands), S. Acosta (Sweden), F. Bastos Goncalves (Portugal), T. Kölbel (Germany), J.J. Kolkman (The Netherlands), T. Lees (UK), J.H. Lefevre (France), G. Menyhei (Hungary), G. Oderich (USA).
    G. Menyhei
    Footnotes
    a Writing Committee: M. Björck∗ (Chair) (Sweden), M. Koelemay (Co-chair) (The Netherlands), S. Acosta (Sweden), F. Bastos Goncalves (Portugal), T. Kölbel (Germany), J.J. Kolkman (The Netherlands), T. Lees (UK), J.H. Lefevre (France), G. Menyhei (Hungary), G. Oderich (USA).
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  • Author Footnotes
    a Writing Committee: M. Björck∗ (Chair) (Sweden), M. Koelemay (Co-chair) (The Netherlands), S. Acosta (Sweden), F. Bastos Goncalves (Portugal), T. Kölbel (Germany), J.J. Kolkman (The Netherlands), T. Lees (UK), J.H. Lefevre (France), G. Menyhei (Hungary), G. Oderich (USA).
    G. Oderich
    Footnotes
    a Writing Committee: M. Björck∗ (Chair) (Sweden), M. Koelemay (Co-chair) (The Netherlands), S. Acosta (Sweden), F. Bastos Goncalves (Portugal), T. Kölbel (Germany), J.J. Kolkman (The Netherlands), T. Lees (UK), J.H. Lefevre (France), G. Menyhei (Hungary), G. Oderich (USA).
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  • Author Footnotes
    b ESVS Guidelines Committee: P. Kolh (Chair) (Belgium), G.J. de Borst (Co-chair and Review Coordinator) (The Netherlands), N. Chakfe (France), S. Debus (Germany), R. Hinchliffe (UK), S. Kakkos (Greece, UK), I. Koncar (Serbia), J. Sanddal Lindholt (Denmark), M. Vega de Ceniga (Spain), F. Vermassen (Belgium), F. Verzini (Italy).
    ESVS Guidelines Committee
    Footnotes
    b ESVS Guidelines Committee: P. Kolh (Chair) (Belgium), G.J. de Borst (Co-chair and Review Coordinator) (The Netherlands), N. Chakfe (France), S. Debus (Germany), R. Hinchliffe (UK), S. Kakkos (Greece, UK), I. Koncar (Serbia), J. Sanddal Lindholt (Denmark), M. Vega de Ceniga (Spain), F. Vermassen (Belgium), F. Verzini (Italy).
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  • P. Kolh
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  • G.J. de Borst
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  • N. Chakfe
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  • S. Debus
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  • R. Hinchliffe
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  • S. Kakkos
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  • I. Koncar
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  • J. Sanddal Lindholt
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  • M. Vega de Ceniga
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  • F. Vermassen
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  • F. Verzini
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  • Author Footnotes
    c Document Reviewers: B. Geelkerken (The Netherlands), P. Gloviczki (USA), T. Huber (USA), R. Naylor (UK).
    Document Reviewers
    Footnotes
    c Document Reviewers: B. Geelkerken (The Netherlands), P. Gloviczki (USA), T. Huber (USA), R. Naylor (UK).
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  • B. Geelkerken
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  • P. Gloviczki
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  • T. Huber
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  • R. Naylor
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  • Author Footnotes
    a Writing Committee: M. Björck∗ (Chair) (Sweden), M. Koelemay (Co-chair) (The Netherlands), S. Acosta (Sweden), F. Bastos Goncalves (Portugal), T. Kölbel (Germany), J.J. Kolkman (The Netherlands), T. Lees (UK), J.H. Lefevre (France), G. Menyhei (Hungary), G. Oderich (USA).
    b ESVS Guidelines Committee: P. Kolh (Chair) (Belgium), G.J. de Borst (Co-chair and Review Coordinator) (The Netherlands), N. Chakfe (France), S. Debus (Germany), R. Hinchliffe (UK), S. Kakkos (Greece, UK), I. Koncar (Serbia), J. Sanddal Lindholt (Denmark), M. Vega de Ceniga (Spain), F. Vermassen (Belgium), F. Verzini (Italy).
    c Document Reviewers: B. Geelkerken (The Netherlands), P. Gloviczki (USA), T. Huber (USA), R. Naylor (UK).
    [email protected]
      Dr Paola De Rango, July 28, 1966 – February 21, 2016

      Keywords

      List of abbreviations

      AAA
      abdominal aortic aneurysm
      ACS
      abdominal compartment syndrome
      AMI
      acute mesenteric ischaemia
      APLAS
      antiphospholipid antibody syndrome
      CA
      coeliac artery
      CMI
      chronic mesenteric ischaemia
      CO
      cardiac output
      CRP
      C-reactive protein
      CTA
      computed tomography angiography
      DSA
      digital subtraction angiography
      DUS
      duplex ultrasound
      EDV
      end-diastolic velocity
      ePTFE
      expanded polytetrafluoroethylene
      ESVS
      European Society for Vascular Surgery
      GWC
      guideline writing committee
      HA
      hepatic artery
      IAH
      intra-abdominal hypertension
      IAP
      Intra-abdominal pressure
      ICU
      intensive care unit
      I-FABP
      intestinal fatty acid binding globulin
      IMA
      inferior mesenteric artery
      IMAD
      isolated mesenteric artery dissections
      JAK2
      Janus-activated kinase gain of function substitute of valine to phenylalanine at position 617
      LMWH
      low molecular weight heparin
      MALS
      median arcuate ligament syndrome (the synonym coeliac artery compression syndrome, CACS, is not used in these guidelines)
      MRA
      magnetic resonance angiography
      MVT
      mesenteric venous thrombosis (often associated with mesenteric venous ischaemia)
      NOMI
      non-occlusive mesenteric ischaemia
      NOAC
      new oral anticoagulants (also named direct oral anticoagulants - DOAC)
      PP
      primary patency
      PROM
      patient reported outcome measure
      PSV
      peak systolic velocity
      PV
      portal vein
      PVT
      portal vein thrombosis
      RCT
      randomised controlled trial
      ROMS
      retrograde open mesenteric artery stenting
      RRT
      renal replacement therapy
      rtPA
      recombinant tissue plasminogen activator
      SA
      splenic artery
      SMA
      superior mesenteric artery
      SMV
      superior mesenteric vein
      SV
      splenic vein
      TBAD
      type B aortic dissection
      TIPS
      transjugular intrahepatic portosystemic shunting
      VKA
      vitamin K antagonist
      WSACS
      World Society of the Abdominal Compartment Syndrome

      1. Introduction and general aspects

      1.1 Introduction and methods

      Members of this Guideline Writing Committee (GWC) were selected by the European Society for Vascular Surgery (ESVS) to represent physicians involved in the management of patients with diseases of the mesenteric arteries and veins. The members of the GWC have provided disclosure statements of all relationships that might be perceived as real or potential sources of conflict of interest. These disclosure forms are kept on file at the headquarters of the ESVS. The GWC report did not receive financial support from any pharmaceutical, device, or surgical company.
      The ESVS Guidelines Committee was responsible for the endorsement process of this guideline. All experts involved in the GWC have approved the final document. All versions of the guideline were reviewed internally by the GWC and the ESVS Guidelines Committee, externally by invited external reviewers, and approved by the Editors of the European Journal of Vascular and Endovascular Surgery.

      1.1.1 The purpose of these guidelines

      The ESVS has developed clinical practice guidelines for the care of patients with diseases of the mesenteric arteries and veins, with the aim of assisting physicians in selecting the best management strategy. This guideline, established by members of the GWC, who are members of the ESVS or non-members with specific expertise in the field, is based on scientific evidence completed with expert opinion on the matter. By summarising and evaluating the best available evidence, recommendations for the evaluation and treatment of patients have been formulated.
      The recommendations are valid only at the time of publication, as technology and disease knowledge in this field changes rapidly and recommendations can become outdated. It is an aim of the ESVS to revise the guidelines every 3 years or when important new insights in the evaluation and management of diseases of the mesenteric arteries and veins become available.
      Although guidelines have the purpose of promoting a standard of care according to specialists in the field, under no circumstance should this guideline be seen as the legal standard of care in all patients. As the word “guideline” implies, the document is a guiding principle, but the care given to a single patient is always dependent on the individual patient (symptom variability, comorbidities, age, level of activity, etc.), treatment setting (techniques available), and other factors.

      1.2 Methodology

      1.2.1 Strategy

      The GWC was convened on October 9, 2015 during a meeting in Brussels. At that meeting the tasks in creating the guideline were evaluated and distributed among the committee members. The same methodology for guideline development, as proposed by the ESVS guideline committee, was followed as for the development of ESVS guidelines for venous disease.
      • Wittens C.
      • Davies A.H.
      • Baekgaard N.
      • Broholm R.
      • Cavezzi A.
      • Chastanet S.
      • et al.
      Editor's choice - Management of chronic venous disease: clinical practice guidelines of the European Society for Vascular Surgery (ESVS).
      The final version of the guideline was submitted on November 26, 2016.

      1.2.2 Literature search and selection

      Members of the GWC, supported by clinical librarians performed the literature search for this guideline systematically in Medline (through PubMed), Embase, Cinahl, and the Cochrane Library up to December 1, 2015. Reference checking and hand search by the GWC members added other relevant literature. A second literature search on papers published between 2015 and 2016 was performed in August 2016. The members of the GWC performed the literature selection based on information provided in the title and abstract of the retrieved studies.
      Several relevant articles published after the search date or in another language were included, but only if they were of paramount importance to this guideline.
      Tabled 1
      Languages:English, German, and French
      Level of evidence:Selection of the literature was performed following the pyramid of evidence, with aggregated evidence in the top of the pyramid (multiple randomised trials, meta-analyses), then single randomised controlled trials, then observational studies (Table 1). Single case reports, animal studies, and in vitro studies were excluded, leaving expert opinions at the bottom of the pyramid. The level of evidence per section in the guideline is dependent on the level of evidence available on the specific subject.
      Sample size:If there were relatively large studies available, with a minimum of 20 subjects per research group, only these were included. If not available, smaller studies were also included.

      1.2.3 Weighing the evidence

      To define the current guidelines, members of the GWC reviewed and summarised the selected literature. Conclusions were drawn based on the scientific evidence.
      The recommendations in these guidelines are based on the European Society of Cardiology grading system.
      • Windecker S.
      • Kolh P.
      • Alfonso F.
      • Collet J.P.
      • Cremer J.
      • Falk V.
      • et al.
      2014 ESC/EACTS Guidelines on myocardial revascularization: the task force on myocardial revascularization of the European Society of Cardiology (ESC) and the European Association for Cardio-Thoracic Surgery (EACTS). Developed with the special contribution of the European Association of Percutaneous Cardiovascular Interventions (EAPCI).
      For each recommendation, the letter A, B, or C marks the level of current evidence (Table 1). Weighing the level of evidence and expert opinion, every recommendation is subsequently marked as class I, IIa, IIb, or III (Table 2). More information on the process of how guidelines are developed by the ESVS can be found on the ESVS web-site (esvs.org).
      Table 1Levels of evidence.
      Table thumbnail fx1
      Table 2Classes of recommendations.
      Table thumbnail fx2

      1.3 Terminology and definitions

      The commonly used nomenclature is confusing, and for this guideline choices have had to be made. For a disease that is under-appreciated, recognition is important. Well-established terms were therefore chosen over ‘anatomically more correct’ terms. Thus, ‘mesenteric’ and not ‘splanchnic’ was used to indicate the coeliac artery (CA), the superior (SMA) and inferior mesenteric arteries (IMA), and ischaemia in that region, as it is used five times more often in the literature. Diseases of the renal arteries are not covered by these guidelines.
      Mesenteric disease can be divided according to three characteristics: (i) presence of symptoms (or not); (ii) clinical presentation: acute, chronic, and acute on chronic ischaemia; and (iii) vessel involvement (the identification and number of involved arteries, venous obstruction, or external compression).
      Acute mesenteric ischaemia (AMI) is defined as the occurrence of an abrupt cessation of the mesenteric blood flow with development of symptoms that may vary in time of onset from minutes (in embolism) to hours (in athero-thrombosis). The leading symptom is severe abdominal pain that may progress to bowel necrosis and peritonitis in days, if left untreated.
      Chronic mesenteric ischaemia (CMI) is defined as ischaemic symptoms caused by insufficient blood supply to the gastrointestinal tract with a duration of at least 3 months. The typical presentation includes postprandial pain, weight loss resulting from fear of eating, or unexplained diarrhoea.
      Acute on chronic ischaemia is defined as AMI in patients who previously had typical symptoms of CMI. Often, the symptoms of CMI worsened over the preceding weeks with periods of prolonged and more severe pain, pain even without eating, onset of diarrhoea, or inability to eat at all.
      Mesenteric ischaemia can be caused by obstruction of arteries and/or veins, and by vasoconstriction of structurally normal vessels: non-occlusive mesenteric ischaemia (NOMI).
      The main causes of mesenteric arterial obstruction are atherosclerotic disease, athero-thrombosis, arterial dissection, and arterial embolism. The main sources of embolism are the heart, especially in atrial fibrillation, and the aortic arch. Vasculitis of the mesenteric vasculature is rare, and can lead to abdominal complaints and bowel infarction, but this condition is not covered by these guidelines. Extrinsic compression of the mesenteric vessels can be caused by the crura of the diaphragm, or by tumour invasion, especially in pancreatic cancer. Congenital malformations (such as the mid-aortic syndrome or gut malrotation), and strangulation resulting from hernia are not covered by these guidelines.
      NOMI is the ultimate consequence of circulatory failure. During low flow states blood flow is redistributed to maintain perfusion of vitally important organs (brain, kidneys, and heart), at the expense of the mesenteric circulation. The clinical scenarios include heart and aortic surgery, abdominal compartment syndrome (ACS), as well as all shock states. This condition is prevalent in critically ill patients.
      The main causes of AMI are embolism, athero-thrombosis, NOMI, and dissection. In CMI atherosclerosis is the predominant cause.
      Symptomatic or asymptomatic compression of the CA is referred to as the median arcuate ligament syndrome (MALS), which is a synonym for coeliac axis compression syndrome.
      Arterial aneurysms may be either true or false. True aneurysms are usually caused by weakening of the vessel wall and dilatation with involvement of all three wall layers. A pseudoaneurysm, or false aneurysm, can develop after injury to the vessel wall or a penetrating atherosclerotic ulcer, and the blood leakage is confined to the vessel wall by surrounding tissue. Causes of aneurysmal degeneration in the mesenteric circulation include traumatic or inflammatory injury (e.g. in pancreatitis), as well as high flow in dilated collaterals. Aneurysms may become symptomatic by thrombosis, embolism, or rupture.
      Venous mesenteric ischaemia is usually caused by thrombosis, and consequently is usually referred to as mesenteric venous thrombosis (MVT), and these are often used as synonymous terms. In these guidelines MVT is used. The causes of MVT include intra-abdominal inflammatory conditions and malignancy, thrombophilic disorders, trauma, and myeloproliferative (haematological) neoplasms. In this guideline MVT is referred to for thrombosis of mesenteric veins, which may be associated with splenic and portal vein thrombosis. Isolated thrombosis of the hepatic veins, the Budd-Chiari syndrome, isolated portal vein thrombosis (very seldom associated with mesenteric ischaemia), and aneurysms of the portal vein, are not covered by these guidelines.

      1.4 Epidemiology

      Mesenteric ischaemia is a group of disorders with incidence rates that may vary according to the acute or chronic presentation and the aetiology (arterial, non-occlusive, venous).
      It has been estimated that around 1% of all patients with an acute abdomen have arterial AMI.
      • Klar E.
      • Rahmanian P.B.
      • Bucker A.
      • Hauenstein K.
      • Jauch K.W.
      • Luther B.
      Acute mesenteric ischemia: a vascular emergency.
      The incidence increases exponentially with age and AMI is the cause of acute abdomen in up to 10% of patients aged over 70 years. The prevalence of acute mesenteric occlusion among patients with an acute abdomen may vary from 2.1% in suspected appendicitis to 17.7% in emergency laparotomy and 31.0% in laparotomy for non-trauma patients.
      • Khan A.
      • Hsee L.
      • Mathur S.
      • Civil I.
      Damage-control laparotomy in nontrauma patients: review of indications and outcomes.
      Cardiac failure, a history of atrial fibrillation, peripheral artery occlusions, and recent surgery have all been associated with an increased incidence.
      • Klar E.
      • Rahmanian P.B.
      • Bucker A.
      • Hauenstein K.
      • Jauch K.W.
      • Luther B.
      Acute mesenteric ischemia: a vascular emergency.
      • Acosta S.
      Mesenteric ischemia.
      Reports on the incidence based on hospital admissions associated with AMI may have underestimated the prevalence of the disease. In a study based on a high autopsy rate (87%) an overall incidence rate of AMI of 12.9/100,000 person years was estimated in the population of Malmö, Sweden between 1970 and 1982, diagnosed either at autopsy or operation. Arterial thromboembolic occlusion was the most common type found in approximately 68% of acute cases with an embolism to thrombosis ratio of 1.4:1 based on autopsy results.
      • Acosta S.
      • Ogren M.
      • Sternby N.H.
      • Bergqvist D.
      • Bjorck M.
      Clinical implications for the management of acute thromboembolic occlusion of the superior mesenteric artery: autopsy findings in 213 patients.
      A recent study from Finland reported an incidence rate of AMI of 7.3/100,000 person years, with a 65% arterial, 28% venous and 7% non-occlusive aetiology.
      • Karkkainen J.M.
      • Lehtimaki T.T.
      • Manninen H.
      • Paajanen H.
      Acute mesenteric ischemia is a more common cause than expected of acute abdomen in the elderly.
      Contemporary incidences of CMI and NOMI are unknown, as only case series or incidences in treated patients have been reported. CMI accounts for less than 1 per 100,000 admissions, but there has been a steady increase in recent years in the USA.
      • Mitchell E.L.
      • Moneta G.L.
      Mesenteric duplex scanning.
      • Schermerhorn M.L.
      • Giles K.A.
      • Hamdan A.D.
      • Wyers M.C.
      • Pomposelli F.B.
      Mesenteric revascularization: management and outcomes in the United States, 1988–2006.
      However, these figures may simply reflect an increasing number of re-interventions in recent years rather than an actual increase in the prevalence. Indeed, because atherosclerosis is the most common cause, the majority of patients have no symptoms and the development of CMI may take months or years to become clinically apparent and the diagnosis to become clear. In patients with known atherosclerotic disease, the prevalence may range from 8% to 70% and a >50% stenosis of more than one mesenteric artery may be detected in up to 15% of cases. Specifically, in patients with abdominal aortic aneurysms (AAA) and peripheral artery disease, a significant stenosis or occlusion of at least one mesenteric artery may be found in around 40% and 25–29%, respectively.
      • Thomas J.H.
      • Blake K.
      • Pierce G.E.
      • Hermreck A.S.
      • Seigel E.
      The clinical course of asymptomatic mesenteric arterial stenosis.
      MVT is a rare condition that accounts for 6–28% of all the cases of AMI and 1 in 1000 emergency department admissions,
      • Kumar S.
      • Sarr M.G.
      • Kamath P.S.
      Mesenteric venous thrombosis.
      • Singal A.K.
      • Kamath P.S.
      • Tefferi A.
      Mesenteric venous thrombosis.
      but it can also cause CMI. The mean age of patients at presentation is 45–60 years with a slight male to female preponderance. The overall incidence of MVT in the Swedish population between 1970 and 1982 was estimated to be 2 per 100,000 compared with 2.7 per 100,000 between 2000 and 2006.
      • Acosta S.
      Epidemiology of mesenteric vascular disease: clinical implications.
      In Finland the incidence of acute MVT was 0.5/100,000 person years.
      • Karkkainen J.M.
      • Lehtimaki T.T.
      • Manninen H.
      • Paajanen H.
      Acute mesenteric ischemia is a more common cause than expected of acute abdomen in the elderly.
      However, the incidence is probably underestimated, given the heterogeneous clinical presentation and the rate of asymptomatic incidental findings. The widespread use of abdominal imaging, in particular computed tomography angiography (CTA), results in an increasing number of cases being diagnosed incidentally. The prevalence of incidentally detected abdominal venous thrombosis, has been reported to be 45/2619 (1.74%, 95% CI 1.29–2.34%).
      • Ageno W.
      • Squizzato A.
      • Togna A.
      • Magistrali F.
      • Mangini M.
      • Fugazzola C.
      • et al.
      Incidental diagnosis of a deep vein thrombosis in consecutive patients undergoing a computed tomography scan of the abdomen: a retrospective cohort study.
      Some 26 patients had portal vein thrombosis (PVT) and eight had symptomatic MVT. MVT and PVT are the most common causes of mesenteric venous ischaemia. PVT was found 10 times more often than MVT at autopsy, but these cases were often asymptomatic, and were seldom considered to be the cause of death.
      • Ogren M.
      • Bergqvist D.
      • Bjorck M.
      • Acosta S.
      • Eriksson H.
      • Sternby N.H.
      Portal vein thrombosis: prevalence, patient characteristics and lifetime risk: a population study based on 23,796 consecutive autopsies.
      In Table 5, (page 31) diagnostic differentiation among venous, arterial occlusive, and non-occlusive mesenteric ischaemia is summarised.
      True aneurysms of the mesenteric arteries and its branches are not common, with an estimated prevalence of 0.1–2%.
      • Fankhauser G.T.
      • Stone W.M.
      • Naidu S.G.
      • Oderich G.S.
      • Ricotta J.J.
      • Bjarnason H.
      • et al.
      The minimally invasive management of visceral artery aneurysms and pseudoaneurysms.
      • Pulli R.
      • Fargion A.
      • Pratesi G.
      • Dorigo W.
      • Angiletta D.
      • Pratesi C.
      Aortic type B dissection with acute expansion of iliac artery aneurysm in previous endovascular repair with iliac branched graft.
      • Saltzberg S.S.
      • Maldonado T.S.
      • Lamparello P.J.
      • Cayne N.S.
      • Nalbandian M.M.
      • Rosen R.J.
      • et al.
      Is endovascular therapy the preferred treatment for all visceral artery aneurysms?.
      With the increasing use of abdominal imaging, the majority are asymptomatic at diagnosis. The true prevalence of pseudoaneurysms is not well defined, but they are more common in patients with acute or chronic abdominal inflammatory or infectious conditions, abdominal trauma, and after hepatobiliary interventions.
      • Huang Y.K.
      • Hsieh H.C.
      • Tsai F.C.
      • Chang S.H.
      • Lu M.S.
      • Ko P.J.
      Visceral artery aneurysm: risk factor analysis and therapeutic opinion.
      • Lagana D.
      • Carrafiello G.
      • Mangini M.
      • Dionigi G.
      • Caronno R.
      • Castelli P.
      • et al.
      Multimodal approach to endovascular treatment of visceral artery aneurysms and pseudoaneurysms.

      1.5 Anatomy and pathophysiology

      The mesenteric arteries include the three ventral branches of the abdominal aorta, supplying blood flow to the viscera. The anatomy of the mesenteric arteries shows great variability, in particular the CA.
      • Debus E.S.
      • Muller-Hulsbeck S.
      • Kolbel T.
      • Larena-Avellaneda A.
      Intestinal ischemia.
      • Douard R.
      • Chevallier J.M.
      • Delmas V.
      • Cugnenc P.H.
      Clinical interest of digestive arterial trunk anastomoses.
      The CA is the most proximal mesenteric artery followed distally by the SMA and the IMA. The CA originates from the distal thoracic or proximal abdominal aorta, at the level of the diaphragm, often with an up to 2 cm course parallel to the aorta. The arterial blood supply of the bowel is characterised by extensive collateralisation, which varies considerably and requires individual assessment. The CA and the SMA are connected by the pancreaticoduodenal arteries described by Rio Branco and by Bühler
      • Douard R.
      • Chevallier J.M.
      • Delmas V.
      • Cugnenc P.H.
      Clinical interest of digestive arterial trunk anastomoses.
      (Fig. 1). The SMA and the IMA are anastomosed by the Riolan and the Villemin arcades at a central mesenteric level, while the marginal arcade of Drummond is peripheral, close to the intestine.
      • Douard R.
      • Chevallier J.M.
      • Delmas V.
      • Cugnenc P.H.
      Clinical interest of digestive arterial trunk anastomoses.
      These macroscopic anastomoses between the three major vessels create a significant tolerance for central obstructions of the vessels: each one has the ability to supply the entire viscera with the help of these anastomoses depending on the rate of the obstructive process. The Sudeck point describes the junction in the recto-sigmoid region, where arterial blood supply changes from the most distal branches of the IMA to the branches of the internal iliac artery. This segment is most prone to colonic ischaemia.
      Figure 1
      Figure 1Collateral arcades between the main mesenteric arterial trunks: the pancreaticoduodenal arcades described by Rio Branco and Bühler between the superior mesenteric artery and the coeliac trunk; the Riolan, Villemin, and Drummond arcades between the inferior and superior mesenteric arteries. The mesenteric artery ends with the superior rectal arteries which originate from the internal iliac arteries via the middle rectal arteries.
      On a microscopic level a capillary network in the submucosal layer provides blood supply to the villi and microvilli of the intestine, which is the most metabolically active layer. This network also includes anastomoses at the base of the villi, which allow redirection of a compromised blood flow away from the mucosa while continuing to perfuse the muscularis and serosa, leading to ischaemic necrosis of the mucosa but preserving the integrity of the bowel, which may be life saving.
      • Parks D.A.
      • Jacobson E.D.
      Physiology of the splanchnic circulation.
      This adaptive principle is known as the counter current mechanism.
      • Lundgren O.
      Studies on blood flow distribution and countercurrent exchange in the small intestine.
      The viscera receive 10–20% of the cardiac output (CO) in the resting state, and 35% postprandially starting 10–30 minutes after a meal and continuing for up to 3 hours to meet the increased metabolic demand.
      • Mitchell E.L.
      • Moneta G.L.
      Mesenteric duplex scanning.
      • Zeller T.
      • Macharzina R.
      Management of chronic atherosclerotic mesenteric ischemia.
      At the start of the meal the CA flow increases and returns to baseline within an hour. The SMA flow increases after the meal, peaks in the first hour and returns to baseline after 2–3 hours.
      • Someya N.
      • Endo M.Y.
      • Fukuba Y.
      • Hayashi N.
      Blood flow responses in celiac and superior mesenteric arteries in the initial phase of digestion.
      The arterial perfusion is regulated by various intrinsic and extrinsic factors with overlapping controls and restrictions such as the autonomic nervous regulation, the haemodynamic condition, local metabolites and hormones.
      • Parks D.A.
      • Jacobson E.D.
      Physiology of the splanchnic circulation.
      Venous drainage of the viscera does not impact on blood flow under normal physiological conditions. However, an increase in the resistance of the venous outflow can significantly influence hydrostatic pressure and fluid balance in the intestines.
      • Parks D.A.
      • Jacobson E.D.
      Physiology of the splanchnic circulation.
      Mesenteric ischaemia is predominantly caused by atherosclerosis affecting the ostia of the mesenteric arteries.
      • Mitchell E.L.
      • Moneta G.L.
      Mesenteric duplex scanning.
      • Debus E.S.
      • Muller-Hulsbeck S.
      • Kolbel T.
      • Larena-Avellaneda A.
      Intestinal ischemia.
      • Zeller T.
      • Macharzina R.
      Management of chronic atherosclerotic mesenteric ischemia.
      These lesions are often associated with other manifestations of atherosclerotic disease, such as coronary artery disease.
      • van Bockel J.H.
      • Geelkerken R.H.
      • Wasser M.N.
      Chronic splanchnic ischaemia.
      • Veenstra R.P.
      • ter Steege R.W.
      • Geelkerken R.H.
      • Huisman A.B.
      • Kolkman J.J.
      The cardiovascular risk profile of atherosclerotic gastrointestinal ischemia is different from other vascular beds.
      MALS, external compression of the coeliac artery by the median arcuate ligament is a common, but mostly asymptomatic, finding. When causing symptoms of postprandial intestinal ischaemia, MALS is also known as the Dunbar syndrome. The clinical significance of this external compression, which may even lead to occlusion of the CA remains unclear, although case series of successful treatment have been reported.
      • Mitchell E.L.
      • Moneta G.L.
      Mesenteric duplex scanning.
      • Mensink P.B.
      • van Petersen A.S.
      • Geelkerken R.H.
      • Otte J.A.
      • Huisman A.B.
      • Kolkman J.J.
      Clinical significance of splanchnic artery stenosis.
      Less common causes of mesenteric occlusive disease include previous arterial embolism, arterial dissection, fibromuscular dysplasia, vasculitis, Takayasu's disease, Cogan's syndrome and Behçet's disease. NOMI is characterised by incomplete interruption of intestinal perfusion caused by hypoperfusion, secondary to low CO, often combined with arterial spasm.
      • Bjorck M.
      • Wanhainen A.
      Nonocclusive mesenteric hypoperfusion syndromes: recognition and treatment.
      True aneurysms and pseudoaneurysms in the mesenteric arteries are most common in the splenic, hepatic, and coeliac arteries. Pseudoaneurysms are caused by iatrogenic injury, trauma, or pancreatitis.
      • Lu M.
      • Weiss C.
      • Fishman E.K.
      • Johnson P.T.
      • Verde F.
      Review of visceral aneurysms and pseudoaneurysms.
      • Shanley C.J.
      • Shah N.L.
      • Messina L.M.
      Common splanchnic artery aneurysms: splenic, hepatic, and celiac.

      1.6 Intestinal salvage

      This section summarises some fundamental principles in saving as much of the threatened bowel as possible, an inter-disciplinary collaboration engaging many groups of surgeons. More details and references are given in Chapter 2, on AMI.
      A general surgical principle is to perform laparotomy in the presence of peritonitis, and mesenteric ischaemia is no exception to this rule.
      • Person B.
      • Dorfman T.
      • Bahouth H.
      • Osman A.
      • Assalia A.
      • Kluger Y.
      Abbreviated emergency laparotomy in the non-trauma setting.
      In the era before CTA and endovascular treatment, AMI could only be reliably diagnosed by laparotomy. Treatment consisted of removal of all necrotic bowel first, with the aim of performing open revascularisation later. In many centres this policy is still the dominant approach. As the diagnosis is now usually made by CTA it has been strongly argued, however, that this approach should be changed and blood flow should be restored as a first step, and then as a second step bowel viability should be assessed and any necrotic bowel resected.
      • Acosta S.
      Mesenteric ischemia.
      • Roussel A.
      • Castier Y.
      • Nuzzo A.
      • Pellenc Q.
      • Sibert A.
      • Panis Y.
      • et al.
      Revascularization of acute mesenteric ischemia after creation of a dedicated multidisciplinary center.
      • Acosta S.
      • Bjorck M.
      Modern treatment of acute mesenteric ischaemia.
      How the revascularisation should take place is dealt with in later chapters of these guidelines.
      Generally speaking, AMI patients should be treated in centres with experience in both open and endovascular revascularisation,
      • Acosta S.
      • Bjorck M.
      Modern treatment of acute mesenteric ischaemia.
      and performing laparotomy first may add to the duration of the AMI. Experience is crucial, because although the number of patients treated by endovascular means for mesenteric ischaemia is rapidly increasing,
      • Schermerhorn M.L.
      • Giles K.A.
      • Hamdan A.D.
      • Wyers M.C.
      • Pomposelli F.B.
      Mesenteric revascularization: management and outcomes in the United States, 1988–2006.
      it is still a relatively rare disorder. It has been suggested that in centres where these options are not available, it would be reasonable to perform bowel resection first, and transport the patient thereafter to a vascular centre. The disadvantages of this policy are: first, the extra hours it takes to perform laparotomy without revascularisation are lost as far as restoring blood flow is concerned; second, it is often difficult to distinguish between reversible and irreversible ischaemic bowel, especially before revascularisation, carrying the risk of resecting potentially viable bowel. When deciding how to manage the patient with AMI, these considerations have to be weighed against the logistical challenges of transporting a seriously ill patient.
      In patients with AMI and signs of peritonitis, laparotomy is mandatory. All gangrenous bowel must be removed. Anastomoses are not recommended in this emergency setting because of a major risk of leakage. Bowel with no obvious sign of necrosis should be left in the abdomen and the viability should be assessed at a second look laparotomy.
      • Acosta S.
      Mesenteric ischemia.
      • Roussel A.
      • Castier Y.
      • Nuzzo A.
      • Pellenc Q.
      • Sibert A.
      • Panis Y.
      • et al.
      Revascularization of acute mesenteric ischemia after creation of a dedicated multidisciplinary center.
      The length of the remaining bowel should be measured at each procedure.
      After extensive small bowel necrosis and resection short bowel syndrome may ensue. The remaining small bowel will become hypertrophic with enlarged villi, with increased absorption capacity, a process known as adaptation. This process can take up to 1 year. In some patients, parenteral nutrition may be needed, either for a limited period or indefinitely. As a general rule, the length of small bowel that is sufficient to allow enteral nutrition depends mainly on the ileocaecal valve: 50 cm suffices with and 100 cm without the ileocaecal valve, respectively. Another factor affecting the quality of life in patients with short bowel syndrome is the length of remaining colon.
      It should be kept in mind that the quality of life on home parenteral nutrition is moderate to good,
      • Huisman-de Waal G.
      • Schoonhoven L.
      • Jansen J.
      • Wanten G.
      • van Achterberg T.
      The impact of home parenteral nutrition on daily life-a review.
      and the outcome of intestinal transplantation is slowly improving,
      • Sudan D.
      The current state of intestine transplantation: indications, techniques, outcomes and challenges.
      the latter may therefore become a future possibility for young patients with short bowel syndrome.

      1.7 Benefit versus harm, the patient's perspective

      Although guidelines are written for medical professionals to guide them through the decision process using the best available evidence, there is increasing emphasis on the patient perspective, and rightly so. In other words: patency and clinical success may be central in a guideline, but the quality of life for a specific patient will define the patient's true perspective. The three steps needed to match medical knowledge with a patient's expectation and perspective are: 1) provide information about the risks, benefits, and uncertainties of treatment (this aspect is of particular importance in the elective setting), 2) clarify the individual patient's preferences to personalise these risks and benefits, and 3) aim to apply these insights in a shared decision making process.
      • Joyce K.E.
      • Lord S.
      • Matlock D.D.
      • McComb J.M.
      • Thomson R.
      Incorporating the patient perspective: a critical review of clinical practice guidelines for implantable cardioverter defibrillator therapy.
      It is expected that in most cases of AMI, application of these principles of patient involvement in decision making, or making decisions based on patient preferences and values, will be very difficult because of the urgent nature of the disorder. For example, although there are ample data showing that quality of life with parenteral nutrition is moderate to good,
      • Huisman-de Waal G.
      • Schoonhoven L.
      • Jansen J.
      • Wanten G.
      • van Achterberg T.
      The impact of home parenteral nutrition on daily life-a review.
      this information is often not taken into account in the patient with AMI who on laparotomy has extensive bowel necrosis. In the chronic patient with single vessel stenosis, the uncertainty of a vascular procedure should be discussed. Moreover, a centre's outcome parameters including patency rates, morbidity, and mortality, should be weighed against the risk of non-treatment. Consideration also may need to be given to referring the patient to a centre with greater experience and caseload. In this guideline the GWC has tried to provide available data for the three ‘patient perspective steps’.
      • i)
        Informing the patients
      In AMI it will be very hard to inform patients adequately before commencing treatment, as the patients are very often in a condition that makes it difficult to understand complex information. In this acute situation it is important to discuss the risks and benefits with the relatives. There may be opportunity, however, after this first phase to discuss the options and potential risks and benefits such as the reduced long-term survival in patients having suffered AMI (50% after 5 years
      • Karkkainen J.M.
      • Lehtimaki T.T.
      • Manninen H.
      • Paajanen H.
      Acute mesenteric ischemia is a more common cause than expected of acute abdomen in the elderly.
      ). The moderate to good quality of life on parenteral nutrition
      • Huisman-de Waal G.
      • Schoonhoven L.
      • Jansen J.
      • Wanten G.
      • van Achterberg T.
      The impact of home parenteral nutrition on daily life-a review.
      should be taken into account.
      For patients with chronic ischemia, the benefit of treatment includes pain relief, and improved survival, which should be weighed against the morbidity and mortality associated with treatment.
      • Rheudasil J.M.
      • Stewart M.T.
      • Schellack J.V.
      • Smith 3rd, R.B.
      • Salam A.A.
      • Perdue G.D.
      Surgical treatment of chronic mesenteric arterial insufficiency.
      When making decisions about treatment, patient preferences and life values should be considered alongside the data on potential physiological benefit.
      Patients with mesenteric artery aneurysms may benefit from intervention while asymptomatic, to prevent death from rupture. The majority, however, may be safely observed. This requires detailed information on the potential risks and benefits of repair and may lead to anxiety in patients who are aware of the diagnosis but do not require treatment.
      In highly specialised centres, which receive patients with CMI, it would seem reasonable to develop leaflets that provide objective information on the potential risks, benefits, and harm of intervention. Such information should be easily understandable and ideally be scrutinised by an expert in communication.
      • ii)
        Personalising risks and benefits and clarification of patient preferences
      Providing patients with a broad overview of the risks and benefits, of both treatment and non-treatment, is a daily challenge for all clinicians. In a relatively rare disease like mesenteric ischaemia, assumptions outnumber hard data, making this challenge greater. Many factors may influence the individual patient perspective. These include uncertainty about the future, side effects of drugs, morbidity and mortality of treatment, expected symptom relief, and the chance of improved survival. It is a general observation that most patients are able to make well balanced decisions.
      • iii)
        Shared decision making
      Quite often, no single best solution for a problem is available. Under these circumstances the clinician should provide all the abovementioned data with an emphasis on the patient's perspective to help the patient to make the best decision.

      2. Arterial ischaemia, acute mesenteric ischaemia

      2.1 Introduction

      Acute thromboembolic occlusion of the mesenteric arteries most commonly affects the SMA. Symptomatic acute occlusions of the CA and/or its branches and IMA are rare and very seldom lead to intestinal infarction
      • Acosta S.
      • Ogren M.
      • Sternby N.H.
      • Bergqvist D.
      • Bjorck M.
      Clinical implications for the management of acute thromboembolic occlusion of the superior mesenteric artery: autopsy findings in 213 patients.
      • Acosta S.
      • Ogren M.
      • Sternby N.H.
      • Bergqvist D.
      • Bjorck M.
      Fatal nonocclusive mesenteric ischaemia: population-based incidence and risk factors.
      because of the extensive collateral arterial network from a patent SMA. Spontaneous dissection of the mesenteric arteries is covered in Chapter 7. These guidelines do not cover traumatic occlusion.

      2.2 Diagnosis

      2.2.1 Clinical presentation: embolism

      A high index of suspicion and awareness among physicians who see patients who may have acute thromboembolic occlusion of the SMA is important. A history of previous embolism is common. A major cause of mesenteric embolism is atrial fibrillation. Development of cardiac thrombi also may be associated with valvular disease, a dilated left atrium, recent myocardial infarction, and ventricular dilatation with mural thrombus.
      The typical clinical triad for an acute embolic SMA occlusion is (i) severe abdominal pain with minimal findings on examination (pain out of proportion to clinical signs), (ii) bowel emptying, and (iii) the presence of a source of embolus, most often atrial fibrillation. This clinical triad is, however, not a consistent finding, but was present in 80% of patients in a prospective study.
      • Acosta S.
      • Bjorck M.
      Acute thrombo-embolic occlusion of the superior mesenteric artery: a prospective study in a well defined population.
      The often sudden onset of abdominal pain (phase 1; reversible ischaemia) may decrease in intensity (phase 2), followed by an increase in abdominal pain associated with clinical deterioration and progression towards generalised peritonitis (phase 3; irreversible ischaemia). Every patient with atrial fibrillation and acute abdominal pain should be suspected of having acute SMA embolism.
      The presence of synchronous ischaemic symptoms from other arterial segments such as extremity ischaemia or stroke/transient ischaemic attack may indicate synchronous embolism, which may be a diagnostic aid. In an autopsy series of patients with fatal occlusion of the SMA, 19% had an acute myocardial infarction, 48% had residual cardiac thrombus, and 68% had synchronous embolism, mainly to arteries supplying the brain, abdominal viscera, and legs.
      • Acosta S.
      • Ogren M.
      • Sternby N.H.
      • Bergqvist D.
      • Bjorck M.
      Clinical implications for the management of acute thromboembolic occlusion of the superior mesenteric artery: autopsy findings in 213 patients.
      The embolus may occlude the arterial lumen completely or partially. Emboli tend to lodge at points of normal anatomical narrowing, usually immediately distal to the origin of a major branch. Typically, the embolus lodges a few centimetres distal to the origin of the SMA, sparing the proximal jejunal branches, and thereby allowing preservation of the proximal jejunum.

      2.2.2 Clinical presentation: thrombosis

      At first evaluation acute thrombotic SMA occlusion is more difficult to diagnose than acute embolic SMA occlusion. Thrombosis occurs at areas of severe atherosclerotic narrowing, most often where the SMA and CA originate from the aorta.
      • Acosta S.
      • Ogren M.
      • Sternby N.H.
      • Bergqvist D.
      • Bjorck M.
      Clinical implications for the management of acute thromboembolic occlusion of the superior mesenteric artery: autopsy findings in 213 patients.
      Occlusive atherosclerotic lesions in the SMA are clinically more important, compared with those in the CA. Prior history of other atherosclerotic manifestations such as coronary, cerebrovascular, or peripheral arterial occlusive disease is common. Every patient with such a history together with acute abdominal pain should be suspected of having SMA thrombosis. In a substantial proportion of these patients, progressive atherosclerosis at the SMA origin may have developed over many years, resulting in collateral circulation to the SMA, mainly from the CA and IMA. Dehydration, low CO, and hypercoagulable states are major contributing factors to thrombosis. In the case of a thrombotic occlusion at the origin of the SMA, ischaemia usually develops from the proximal jejunum to the mid-transverse colon.
      In retrospect, a high proportion of the often misunderstood and misdiagnosed patients with acute thrombotic SMA occlusion may have had long-standing pre-existing symptoms of CMI, including postprandial abdominal pain (abdominal angina), fear of eating, diarrhoea, and weight loss. Indeed, 80% of patients were misdiagnosed and inappropriately treated medically with proton pump inhibitors, cortisone, or antibiotics in the diagnostic phase in a recent series.
      • Bjornsson S.
      • Resch T.
      • Acosta S.
      Symptomatic mesenteric atherosclerotic disease-lessons learned from the diagnostic workup.
      This series did not support the view that the majority of these patients suffer from cachexia at diagnosis. Weight loss is a consistent finding in patients with two or three vessel disease. A proportion of patients were overweight when they fell ill; however, decreasing in weight to normal at the time of diagnosis.
      • Bjornsson S.
      • Resch T.
      • Acosta S.
      Symptomatic mesenteric atherosclerotic disease-lessons learned from the diagnostic workup.
      Patients diagnosed with advanced symptomatic CMI should be treated subacutely as transition from CMI to AMI is unpredictable.
      • Acosta S.
      • Bjorck M.
      Modern treatment of acute mesenteric ischaemia.
      • Bjornsson S.
      • Resch T.
      • Acosta S.
      Symptomatic mesenteric atherosclerotic disease-lessons learned from the diagnostic workup.
      Further recommendations regarding this group of patients are given in Chapter 3.

      2.2.3 Laboratory markers

      No plasma marker is accurate for diagnosis in the acute setting.
      • Karkkainen J.M.
      • Lehtimaki T.T.
      • Manninen H.
      • Paajanen H.
      Acute mesenteric ischemia is a more common cause than expected of acute abdomen in the elderly.
      • Acosta S.
      • Nilsson T.K.
      • Bjorck M.
      d-dimer testing in patients with suspected acute thromboembolic occlusion of the superior mesenteric artery.
      • Block T.A.
      • Acosta S.
      • Bjorck M.
      Endovascular and open surgery for acute occlusion of the superior mesenteric artery.
      • Akyildiz H.
      • Akcan A.
      • Ozturk A.
      • Sozuer E.
      • Kucuk C.
      • Karahan I.
      The correlation of the d-dimer test and biphasic computed tomography with mesenteric computed tomography angiography in the diagnosis of acute mesenteric ischemia.
      • Chiu Y.H.
      • Huang M.K.
      • How C.K.
      • Hsu T.F.
      • Chen J.D.
      • Chern C.H.
      • et al.
      d-dimer in patients with suspected acute mesenteric ischemia.
      • Matsumoto S.
      • Sekine K.
      • Funaoka H.
      • Yamazaki M.
      • Shimizu M.
      • Hayashida K.
      • et al.
      Diagnostic performance of plasma biomarkers in patients with acute intestinal ischaemia.
      • Thuijls G.
      • van Wijck K.
      • Grootjans J.
      • Derikx J.P.
      • van Bijnen A.A.
      • Heineman E.
      • et al.
      Early diagnosis of intestinal ischemia using urinary and plasma fatty acid binding proteins.
      • Gearhart S.L.
      • Delaney C.P.
      • Senagore A.J.
      • Banbury M.K.
      • Remzi F.H.
      • Kiran R.P.
      • et al.
      Prospective assessment of the predictive value of alpha-glutathione S-transferase for intestinal ischemia.
      • Block T.
      • Nilsson T.K.
      • Bjorck M.
      • Acosta S.
      Diagnostic accuracy of plasma biomarkers for intestinal ischaemia.
      • Shi H.
      • Wu B.
      • Wan J.
      • Liu W.
      • Su B.
      The role of serum intestinal fatty acid binding protein levels and d-lactate levels in the diagnosis of acute intestinal ischemia.
      • Acosta S.
      • Block T.
      • Bjornsson S.
      • Resch T.
      • Bjorck M.
      • Nilsson T.
      Diagnostic pitfalls at admission in patients with acute superior mesenteric artery occlusion.
      • Park W.M.
      • Gloviczki P.
      • Cherry Jr., K.J.
      • Hallett Jr., J.W.
      • Bower T.C.
      • Panneton J.M.
      • et al.
      Contemporary management of acute mesenteric ischemia: factors associated with survival.
      • Lange H.
      • Jackel R.
      Usefulness of plasma lactate concentration in the diagnosis of acute abdominal disease.
      • Studer P.
      • Vaucher A.
      • Candinas D.
      • Schnuriger B.
      The value of serial serum lactate measurements in predicting the extent of ischemic bowel and outcome of patients suffering acute mesenteric ischemia.
      d-dimer has been found to be a consistent highly sensitive early marker, but the specificity was low. The high sensitivity, approaching 100%, makes it an excellent exclusion test, but many other conditions are associated with high d-dimer values.
      • Acosta S.
      • Nilsson T.K.
      • Bjorck M.
      d-dimer testing in patients with suspected acute thromboembolic occlusion of the superior mesenteric artery.
      • Block T.A.
      • Acosta S.
      • Bjorck M.
      Endovascular and open surgery for acute occlusion of the superior mesenteric artery.
      Hence, a normal d-dimer at presentation most probably excludes acute SMA occlusion. In series with acute SMA occlusion including patients with MVT
      • Akyildiz H.
      • Akcan A.
      • Ozturk A.
      • Sozuer E.
      • Kucuk C.
      • Karahan I.
      The correlation of the d-dimer test and biphasic computed tomography with mesenteric computed tomography angiography in the diagnosis of acute mesenteric ischemia.
      • Chiu Y.H.
      • Huang M.K.
      • How C.K.
      • Hsu T.F.
      • Chen J.D.
      • Chern C.H.
      • et al.
      d-dimer in patients with suspected acute mesenteric ischemia.
      and NOMI,
      • Matsumoto S.
      • Sekine K.
      • Funaoka H.
      • Yamazaki M.
      • Shimizu M.
      • Hayashida K.
      • et al.
      Diagnostic performance of plasma biomarkers in patients with acute intestinal ischaemia.
      the sensitivity for d-dimer has been reported to be around 95%. In a recent publication plasma intestinal fatty acid binding protein (I-FABP) was reported to be much higher among 19 patients with vascular intestinal ischaemia than among 26 patients with non-vascular irreversible intestinal ischaemia.
      • Matsumoto S.
      • Sekine K.
      • Funaoka H.
      • Yamazaki M.
      • Shimizu M.
      • Hayashida K.
      • et al.
      Diagnostic performance of plasma biomarkers in patients with acute intestinal ischaemia.
      Receiver operating characteristics curve analysis suggested that plasma I-FABP was accurate at diagnosing a vascular cause of intestinal ischaemia with an area under the curve of 0.88. Another report found that diagnostic accuracy was better for I-FABP in urine compared with plasma, with an area under the curve of 0.93 versus 0.70, respectively.
      • Thuijls G.
      • van Wijck K.
      • Grootjans J.
      • Derikx J.P.
      • van Bijnen A.A.
      • Heineman E.
      • et al.
      Early diagnosis of intestinal ischemia using urinary and plasma fatty acid binding proteins.
      Currently, no recommendation on the use of I-FABP can be issued, because these very small series need confirmation.
      Figure thumbnail fx3

      2.2.4 Computed tomography angiography

      Diagnosis of acute SMA occlusion and severity of intestinal ischaemia has been greatly facilitated by the evolution and availability of high resolution CTA around the clock.
      • Menke J.
      Diagnostic accuracy of multidetector CT in acute mesenteric ischemia: systematic review and meta-analysis.
      Intravenous contrast enhanced CT with a slice thickness of 1 mm or thinner, performed with and without contrast in both the arterial and portal venous phases (triphasic protocol) is currently recommended as the first line imaging technique to best diagnose occlusive pathology in the arteries and intestinal pathologies, respectively.
      • Oliva I.B.
      • Davarpanah A.H.
      • Rybicki F.J.
      • Desjardins B.
      • Flamm S.D.
      • Francois C.J.
      • et al.
      ACR Appropriateness Criteria (R) imaging of mesenteric ischemia.
      Reconstructions of images in the sagittal, coronal, and transverse planes are often helpful.
      Embolic occlusion often appears as an oval-shaped filling defect surrounded by contrast in a non-calcified arterial segment located in the middle and distal part of the main stem of the SMA. The presence of synchronous emboli to the other visceral, limb, or cerebral arteries is a common finding.
      • Wadman M.
      • Block T.
      • Ekberg O.
      • Syk I.
      • Elmstahl S.
      • Acosta S.
      Impact of MDCT with intravenous contrast on the survival in patients with acute superior mesenteric artery occlusion.
      Increased awareness of the high likelihood of atrial fibrillation related causes for acute abdominal pain may improve diagnostic performance of CTA and triage of patients with acute embolic SMA occlusion.
      • Hunt S.J.
      • Coakley F.V.
      • Webb E.M.
      • Westphalen A.C.
      • Poder L.
      • Yeh B.M.
      Computed tomography of the acute abdomen in patients with atrial fibrillation.
      Thrombotic occlusion usually appears as clot superimposed on a heavily calcified occlusive lesion at the origin of the SMA. The presence of vascular pathology precedes the intestinal pathology, which is of crucial importance when the images are studied.
      • Wadman M.
      • Block T.
      • Ekberg O.
      • Syk I.
      • Elmstahl S.
      • Acosta S.
      Impact of MDCT with intravenous contrast on the survival in patients with acute superior mesenteric artery occlusion.
      Even patients with impaired renal function or increased creatinine values should undergo CTA if there is a suspicion of acute SMA occlusion, accepting the risk of contrast induced renal failure,
      • Acosta S.
      • Bjornsson S.
      • Ekberg O.
      • Resch T.
      CT angiography followed by endovascular intervention for acute superior mesenteric artery occlusion does not increase risk of contrast-induced renal failure.
      to improve diagnostic accuracy and chances of survival.
      If no clinical suspicion of AMI is mentioned in the information provided to the radiologist, the condition is highly likely to be under-diagnosed.
      • Lehtimaki T.T.
      • Karkkainen J.M.
      • Saari P.
      • Manninen H.
      • Paajanen H.
      • Vanninen R.
      Detecting acute mesenteric ischemia in CT of the acute abdomen is dependent on clinical suspicion: review of 95 consecutive patients.
      It is not unusual that a second look at the imaging may detect overlooked radiological findings associated with AMI at the initial reading,
      • Firetto M.C.
      • Lemos A.A.
      • Marini A.
      • Avesani E.C.
      • Biondetti P.R.
      Acute bowel ischemia: analysis of diagnostic error by overlooked findings at MDCT angiography.
      and such diagnostic delay undoubtedly has a negative impact on prognosis. In addition, the radiologists' experience and expertise have an impact on their performance in diagnosing AMI.
      • Blachar A.
      • Barnes S.
      • Adam S.Z.
      • Levy G.
      • Weinstein I.
      • Precel R.
      • et al.
      Radiologists' performance in the diagnosis of acute intestinal ischemia, using MDCT and specific CT findings, using a variety of CT protocols.
      In the absence of intestinal findings on CT or peritonitis on clinical examination, patients with acute abdominal pain and CTA verified occlusion of the SMA are unlikely to be diagnosed in time to allow intestinal revascularisation. Diagnostic accuracy and specificity for CTA in diagnosing acute SMA occlusion is very good, and is superior to any of the plasma biomarker candidates.
      • Cudnik M.T.
      • Darbha S.
      • Jones J.
      • Macedo J.
      • Stockton S.W.
      • Hiestand B.C.
      The diagnosis of acute mesenteric ischemia: a systematic review and meta-analysis.
      Reconstructed images using maximum intensity projection, volume rendering, and multiplanar volume reconstruction have been found to perform better for the detection of vascular abnormalities and to improve the diagnostic confidence of radiologists in the evaluation of bowel and mesenteric abnormalities.
      • Barmase M.
      • Kang M.
      • Wig J.
      • Kochhar R.
      • Gupta R.
      • Khandelwal N.
      Role of multidetector CT angiography in the evaluation of suspected mesenteric ischemia.
      In series of suspected cases with AMI including a high proportion of cases with acute SMA occlusion, the sensitivity of CTA in diagnosing AMI ranged from 73% to 100%, and the specificity from 90% to 100%.
      • Akyildiz H.
      • Akcan A.
      • Ozturk A.
      • Sozuer E.
      • Kucuk C.
      • Karahan I.
      The correlation of the d-dimer test and biphasic computed tomography with mesenteric computed tomography angiography in the diagnosis of acute mesenteric ischemia.
      • Barmase M.
      • Kang M.
      • Wig J.
      • Kochhar R.
      • Gupta R.
      • Khandelwal N.
      Role of multidetector CT angiography in the evaluation of suspected mesenteric ischemia.
      • Aschoff A.J.
      • Stuber G.
      • Becker B.W.
      • Hoffmann M.H.
      • Schmitz B.L.
      • Schelzig H.
      • et al.
      Evaluation of acute mesenteric ischemia: accuracy of biphasic mesenteric multi-detector CT angiography.
      • Kirkpatrick I.D.
      • Kroeker M.A.
      • Greenberg H.M.
      Biphasic CT with mesenteric CT angiography in the evaluation of acute mesenteric ischemia: initial experience.
      • Ofer A.
      • Abadi S.
      • Nitecki S.
      • Karram T.
      • Kogan I.
      • Leiderman M.
      • et al.
      Multidetector CT angiography in the evaluation of acute mesenteric ischemia.
      • Yikilmaz A.
      • Karahan O.I.
      • Senol S.
      • Tuna I.S.
      • Akyildiz H.Y.
      Value of multislice computed tomography in the diagnosis of acute mesenteric ischemia.

      2.2.5 Duplex ultrasound

      Duplex ultrasound (DUS) of the visceral arteries is an operator-dependent imaging modality, and it may not be possible to obtain accurate assessments around the clock. Furthermore, bowel paralysis associated with acute intestinal ischaemia precludes accurate ultrasound scanning in many patients. Although proximal occlusive lesions of the visceral arteries can be identified, distal occlusions cannot. DUS is not an appropriate imaging method to assess acute occlusive lesions of the visceral arteries.

      2.2.6 Digital subtraction angiography

      Figure thumbnail fx4
      In Table 5, (page 31) diagnostic differentiation of venous, arterial occlusive, and non-occlusive mesenteric ischaemia are summarised.

      2.3 Treatment of acute superior mesenteric artery occlusion

      2.3.1 Current approaches

      Intestinal revascularisation is necessary in most patients with acute SMA occlusion. The only situation in which a bowel resection without revascularisation may save the life of the patient is in the case of a distal embolus, with a widely open proximal artery. The extent of intestinal infarction involves the jejunum, ileum, and colon in 50% of the patients, and at least two of these intestinal segments in 82%,
      • Acosta S.
      • Ogren M.
      • Sternby N.H.
      • Bergqvist D.
      • Bjorck M.
      Clinical implications for the management of acute thromboembolic occlusion of the superior mesenteric artery: autopsy findings in 213 patients.
      which means that bowel resection alone would be life saving for a minority of patients. Optimal treatment may include both open and endovascular surgery, and patients are best treated in a vascular centre with a hybrid operating room, although logistical aspects must be taken into consideration in this urgent situation. From pre-operative clinical and radiological evaluation, it should be determined whether or not the patient has peritonitis, and whether the occlusion is embolic or thrombotic. The presence of intestinal wall or porto-mesenteric gas on CTA is a sign of severe transmural ischaemia, but is not necessarily associated with a fatal outcome if treated in a timely fashion.
      • Studer P.
      • Vaucher A.
      • Candinas D.
      • Schnuriger B.
      The value of serial serum lactate measurements in predicting the extent of ischemic bowel and outcome of patients suffering acute mesenteric ischemia.
      Laparotomy is indicated if there are signs of peritonitis and suspicion of intestinal infarction, unless a palliative approach has been chosen. Laparotomy aims to assess the extent and severity of intestinal ischaemia and vessel patency, although the latter may require peri-operative angiography. Laparotomy, rather than laparoscopy, is usually safer and quicker to evaluate the visceral organs. Extensive intestinal paralysis with dilated bowel loops may be impossible to evaluate at laparoscopy, even by an expert. Elderly patients with complete transmural infarction of the small bowel up to the mid-transverse colon would need extensive bowel resection that would lead to short bowel syndrome and increased morbidity. Survival in these patients is poor and surgery may be inappropriate for ethical reasons. In the event of bowel perforation, the affected intestinal segment is resected, leaving the reconstruction of the intestines or stoma formation until a second look laparotomy after 18–36 hours.

      2.3.2 Acute mesenteric arterial revascularisation

      Acute mesenteric arterial revascularisation is preferably done before any bowel surgery, even if there is a limited length of necrotic bowel that could be rapidly resected. If laparotomy has been performed because of an uncertain diagnosis of peritonitis in a hospital where there is no vascular surgeon available, it may be preferable to resect necrotic bowel without reconstruction, close the abdomen, and transport the patient to a vascular centre for revascularisation.
      According to the Swedish National Registry for Vascular Surgery (Swedvasc),
      • Block T.A.
      • Acosta S.
      • Bjorck M.
      Endovascular and open surgery for acute occlusion of the superior mesenteric artery.
      there has been a steady increase in mesenteric revascularisation for AMI since 2004. In 2009, endovascular treatment overtook open surgery in Sweden: 29 endovascular versus 24 open revascularisations. In contrast, this shift in treatment modality has not taken place in North America.
      • Ryer E.J.
      • Kalra M.
      • Oderich G.S.
      • Duncan A.A.
      • Gloviczki P.
      • Cha S.
      • et al.
      Revascularization for acute mesenteric ischemia.
      The 30 day mortality rate in Swedvasc was similar after open versus endovascular surgery for embolic occlusions (37% vs. 33%), whereas the mortality rate was significantly higher after open than endovascular treatment for thrombotic occlusions (56% vs. 23%). Of note, no patient had completion angiography after open surgical treatment, whereas completion angiography is part of the procedure after endovascular surgery. There may have been differences in disease severity between the treatment groups, but it remains possible that the endovascular approach is better for thrombotic occlusions in elderly, frail patients.
      • Block T.A.
      • Acosta S.
      • Bjorck M.
      Endovascular and open surgery for acute occlusion of the superior mesenteric artery.
      There is rarely any indication for revascularisation of both the SMA and the CA, and SMA revascularisation seems to be more important. Even after successful endovascular recanalisation of the mesenteric arteries, patients may still require laparotomy when persisting signs of peritoneal irritation indicate the presence of non-viable bowel.

      2.3.3 Open superior mesenteric artery embolectomy

      Open SMA embolectomy remains a good treatment option.
      • Yun W.S.
      • Lee K.K.
      • Cho J.
      • Kim H.K.
      • Huh S.
      Treatment outcome in patients with acute superior mesenteric artery embolism.
      • Bingol H.
      • Zeybek N.
      • Cingoz F.
      • Yilmaz A.T.
      • Tatar H.
      • Sen D.
      Surgical therapy for acute superior mesenteric artery embolism.
      When laparotomy has been performed in a patient with peritonitis, exposure of the SMA is performed. A 5 cm transverse incision in the visceral peritoneum/transverse mesocolon in the root of the mesentery, just below the body of the pancreas, is performed. If the embolus is distal in the artery, the pulse in the SMA can easily be palpated, and the artery is located dorsally to the left of the often easily recognised superior mesenteric vein (SMV). After arteriotomy, balloon embolectomy with a 3 or 4 Fr Fogarty catheter is indicated. The result should be checked by some form of completion control, such as angiography of the SMA with antero-posterior and lateral views, or transit time flow measurement. If none of these modalities are available, pulse palpation distally in the mesentery can be performed. Comparative data regarding which completion control method to use are lacking. The presence or absence of stenosis and dissection at the arteriotomy closure site, residual peripheral embolus in arterial branches not cleared, and venous return to the portal vein can only be assessed by DSA.

      2.3.4 Open vascular surgery for acute thrombotic superior mesenteric artery occlusion

      Figure thumbnail fx5

      2.3.5 Assessment of bowel viability

      Intestinal ischaemia may be extensive, ranging from lesions in the jejunum, ileum, and colon, to a normal appearance of the serosa. Ischaemic changes are more extensive on the mucosal side. Intestinal ischaemia is characterised by patchy cyanosis, reddish black discolouration, decreased or absent peristalsis, and no palpable pulsation in the mesentery. The use of intra-operative Doppler for detection of pulsatile mural blood flow and intravenous injection of fluorescein for assessment of ultraviolet fluorescence pattern in the assessment of bowel viability has been compared with clinical judgement,
      • Bulkley G.B.
      • Zuidema G.D.
      • Hamilton S.R.
      • O'Mara C.S.
      • Klacsmann P.G.
      • Horn S.D.
      Intraoperative determination of small intestinal viability following ischemic injury: a prospective, controlled trial of two adjuvant methods (Doppler and fluorescein) compared with standard clinical judgment.
      and the fluorescence pattern method was more accurate than both clinical judgement and Doppler. However, the fluorescence pattern method has not been established as the method of choice in a centre that has used both these non-clinical methods.
      • Ryer E.J.
      • Kalra M.
      • Oderich G.S.
      • Duncan A.A.
      • Gloviczki P.
      • Cha S.
      • et al.
      Revascularization for acute mesenteric ischemia.
      The accuracy of laser Doppler flowmetry and clinical assessment was reported to be 100% and 87%, respectively, in one study.
      • Redaelli C.A.
      • Schilling M.K.
      • Buchler M.W.
      Intraoperative laser Doppler flowmetry: a predictor of ischemic injury in acute mesenteric infarction.
      There has been a paucity of studies concerning laser Doppler flowmetry, however, questioning its clinical applicability. None of the described adjunctive methods have become established in clinical practice, which is the reason why no recommendation can be made regarding their applicability. Clinical assessment at laparotomy has remained the preferred method for assessment of bowel viability.
      • Kalra M.
      • Ryer E.J.
      • Oderich G.S.
      • Duncan A.A.
      • Bower T.C.
      • Gloviczki P.
      Contemporary results of treatment of acute arterial mesenteric thrombosis: has endovascular treatment improved outcomes?.
      Figure thumbnail fx6

      2.4 Endovascular therapeutic options in acute mesenteric ischaemia

      2.4.1 Access to the superior mesenteric artery

      The SMA can be reached via the femoral and brachial routes, although sometimes local exposure of the SMA in the abdomen is also needed. Brachial access may be preferable if there is a sharp downward angle between the aorta and the SMA, or if the ostium of the SMA is calcified. If an antegrade approach from the femoral or brachial artery fails, a retrograde approach through the exposed SMA after laparotomy can be attempted, unless open revascularisation is preferred.
      • Acosta S.
      • Sonesson B.
      • Resch T.
      Endovascular therapeutic approaches for acute superior mesenteric artery occlusion.

      2.4.2 Aspiration embolectomy of the superior mesenteric artery

      Endovascular aspiration embolectomy is a treatment option in patients without peritonitis.
      • Wong P.F.
      • Gilliam A.D.
      • Kumar S.
      • Shenfine J.
      • O'Dair G.N.
      • Leaper D.J.
      Antibiotic regimens for secondary peritonitis of gastrointestinal origin in adults.
      • Rotondo M.F.
      • Schwab C.W.
      • McGonigal M.D.
      • Phillips 3rd, G.R.
      • Fruchterman T.M.
      • Kauder D.R.
      • et al.
      ‘Damage control’: an approach for improved survival in exsanguinating penetrating abdominal injury.
      • Acosta S.
      • Sonesson B.
      • Resch T.
      Endovascular therapeutic approaches for acute superior mesenteric artery occlusion.
      • Heiss P.
      • Loewenhardt B.
      • Manke C.
      • Hellinger A.
      • Dietl K.H.
      • Schlitt H.J.
      • et al.
      Primary percutaneous aspiration and thrombolysis for the treatment of acute embolic superior mesenteric artery occlusion.
      • Raupach J.
      • Lojik M.
      • Chovanec V.
      • Renc O.
      • Strycek M.
      • Dvorak P.
      • et al.
      Endovascular management of acute embolic occlusion of the superior mesenteric artery: a 12-year single-centre experience.
      Usually an appropriate catheter and a hydrophilic 0.035 inch guidewire is passed into the ileocolic branch of the SMA. The wire is then replaced with a stiffer wire to achieve stability. With the wire in place, typically an introducer with a removable hub is placed proximal to the embolus in the SMA. Inside this, a smaller guiding catheter
      • Choi K.S.
      • Kim J.D.
      • Kim H.C.
      • Min S.I.
      • Min S.K.
      • Jae H.J.
      • et al.
      Percutaneous aspiration embolectomy using guiding catheter for the superior mesenteric artery embolism.
      • Kawasaki R.
      • Miyamoto N.
      • Oki H.
      • Yamaguchi M.
      • Okada T.
      • Sugimura K.
      • et al.
      Aspiration therapy for acute superior mesenteric artery embolism with an angled guiding sheath and guiding catheter.
      is introduced into the clot, which is aspirated with a 20 mL syringe as the catheter is withdrawn. The hub of the introducer is removed to allow clearance of residual clots. Angiography is performed, usually followed by repeated aspirations. An alternative is to use an over the wire double lumen aspiration catheter, which may allow removal of smaller peripheral clots.

      2.4.3 Local superior mesenteric artery thrombolysis

      In cases of incomplete aspiration embolectomy or distal embolisation, local thrombolysis is a viable treatment alternative in patients without peritonitis.
      • Bjornsson S.
      • Bjorck M.
      • Block T.
      • Resch T.
      • Acosta S.
      Thrombolysis for acute occlusion of the superior mesenteric artery.
      • Yanar F.
      • Agcaoglu O.
      • Sarici I.S.
      • Sivrikoz E.
      • Ucar A.
      • Yanar H.
      • et al.
      Local thrombolytic therapy in acute mesenteric ischemia.
      With the introducer placed in the proximal SMA, a multiple sidehole catheter delivering thrombolytic agents over 10 cm, or an end hole catheter, is advanced to within the embolus. Local thrombolysis is most often achieved by administration of recombinant tissue plasminogen activator (rtPA) at a rate of 0.5–1 mg/h (or other agents, at different dosages, e.g. urokinase 120,000 IU/h), checking the patency with repeated angiograms once or twice per day (Fig. 2A–E). Bleeding complications during local thrombolysis are uncommon and usually self limiting.
      • Bjornsson S.
      • Bjorck M.
      • Block T.
      • Resch T.
      • Acosta S.
      Thrombolysis for acute occlusion of the superior mesenteric artery.
      Small peripheral residual emboli can be treated conservatively with heparin anticoagulation as the marginal arteries in the mesentery may provide sufficient collateral circulation to the affected intestinal segment.
      • Acosta S.
      • Sonesson B.
      • Resch T.
      Endovascular therapeutic approaches for acute superior mesenteric artery occlusion.
      In one large population based study only 38% of patients needed to undergo laparotomy for inspection of the intestines after local thrombolysis.
      • Bjornsson S.
      • Bjorck M.
      • Block T.
      • Resch T.
      • Acosta S.
      Thrombolysis for acute occlusion of the superior mesenteric artery.
      This low occurrence is probably explained by peritonitis or other signs of bowel gangrene being considered as contraindications to thrombolysis. Endovascular rheolytic thromboembolectomy may be a supplementary technique to aspiration thromboembolectomy in cases where thrombolysis is contraindicated.
      Figure 2
      Figure 2Patient with an acute embolic occlusion of the SMA. CTA images in transverse (A), coronal (B), and sagittal (C) projection. The typical oval-shaped embolic occlusion is best seen in the sagittal projection (C). SMA angiography prior to (D) and after (E) local administration of 18 mg of alteplase with clearance of embolus. Laparoscopy was negative, and recovery was uneventful.

      2.4.4 Antegrade recanalisation and stenting of the superior mesenteric artery

      Treatment of underlying stenotic or occlusive lesions is most often achieved during the same procedure, after removal of a thrombotic clot by aspiration or thrombolysis.
      • Acosta S.
      • Sonesson B.
      • Resch T.
      Endovascular therapeutic approaches for acute superior mesenteric artery occlusion.
      The sequence of endovascular intervention versus exploratory laparotomy depends on the clinical state of the patient. When a stable wire has been placed in the ileocolic artery, an introducer is advanced across the atherosclerotic lesion. Balloon expandable stents are better to maintain lumen diameter after stent deployment across hard, calcified ostial lesions than self expanding stents. The balloon expandable stent is placed at the level of the stenosis, followed by retraction of the protective introducer sheath, thus exposing the stent, which is deployed by inflating the balloon. Unfavourable artery angulation or a potential risk of arterial dissection at the distal end of the stent is treated by extension with a self expanding stent into the mid-SMA. Results after stenting are checked by angiography, as well as by pressure measurement. If there is a residual pressure gradient across the stent exceeding 12 mmHg, additional angioplasty and/or stenting is performed.
      • Dias N.V.
      • Acosta S.
      • Resch T.
      • Sonesson B.
      • Alhadad A.
      • Malina M.
      • et al.
      Mid-term outcome of endovascular revascularization for chronic mesenteric ischaemia.

      2.4.5 Retrograde recanalisation and stenting of the superior mesenteric artery

      If percutaneous access fails, laparotomy and exposure of the SMA is performed for retrograde SMA recanalisation and stenting.
      • Acosta S.
      • Sonesson B.
      • Resch T.
      Endovascular therapeutic approaches for acute superior mesenteric artery occlusion.
      • Wyers M.C.
      • Powell R.J.
      • Nolan B.W.
      • Cronenwett J.L.
      Retrograde mesenteric stenting during laparotomy for acute occlusive mesenteric ischemia.
      • Blauw J.T.
      • Meerwaldt R.
      • Brusse-Keizer M.
      • Kolkman J.J.
      • Gerrits D.
      • Geelkerken R.H.
      • et al.
      Retrograde open mesenteric stenting for acute mesenteric ischemia.
      • Chen Y.
      • Zhu J.
      • Ma Z.
      • Dai X.
      • Fan H.
      • Feng Z.
      • et al.
      Hybrid technique to treat superior mesenteric artery occlusion in patients with acute mesenteric ischemia.
      This approach offers the opportunity to inspect the abdominal viscera, to have distal control of the SMA, and to avoid bypass surgery in the setting of necrotic bowel. A puncture is made in the vessel in its main trunk or in one of its major branches with a micro puncture needle; the occlusion is often recanalised easily with a guidewire placed into the aorta. The SMA is clamped distally to avoid distal embolisation if there is fresh thrombus at the occlusion site. The proximal SMA lesion is then crossed with a stiff catheter, exchanging for a hydrophilic guidewire. The wire is snared in the aorta using a snare passed through a brachial or femoral access and then brought out, creating through and through access. An introducer is placed antegradely in the SMA over the through and through wire, followed by stenting. The access puncture in the SMA is treated by manual compression or interrupted suture(s). Antegrade stenting is better than retrograde stenting, because the procedure can be performed with standard devices without exposing the operators to a higher dose of radiation.

      2.4.6 Outcomes after open versus endovascular revascularisation for acute mesenteric ischaemia

      Figure thumbnail fx9
      Figure 3
      Figure 3Meta-analysis of bowel resection rates after open and endovascular therapy of AMI.
      Figure 4
      Figure 4Meta-analysis of 30-day mortality rates after open and endovascular therapy of AMI.

      2.5 Follow-up

      A methodological problem when discussing the data on follow-up after treatment for mesenteric ischaemia is that publications reporting on the risk of restenosis, re-occlusion, and bowel gangrene after treatment focus on the technique that was used (such as stenting) rather than whether the patient suffered acute, chronic, or acute on chronic mesenteric ischaemia.
      In the next chapter (3, on CMI), follow-up after endovascular treatment such as SMA or CA stenting is discussed. Patients who have a stent inserted in the SMA after treatment for CMI or AMI may be followed repeatedly by either DUS or CTA because of the high risk of in-stent restenosis, 36% after a mean follow-up of 29 months.
      • Tallarita T.
      • Oderich G.S.
      • Macedo T.A.
      • Gloviczki P.
      • Misra S.
      • Duncan A.A.
      • et al.
      Reinterventions for stent restenosis in patients treated for atherosclerotic mesenteric artery disease.
      In a large series of patients undergoing endovascular revascularisation for CMI, five patients (3.4%) died during the follow-up period of 64 months because of recurrence of AMI, according to a review of death certificates or autopsy reports.
      • Tallarita T.
      • Oderich G.S.
      • Gloviczki P.
      • Duncan A.A.
      • Kalra M.
      • Cha S.
      • et al.
      Patient survival after open and endovascular mesenteric revascularization for chronic mesenteric ischemia.
      If the risk of dying from AMI is so high after re-occlusion of a stent inserted for CMI, the risk is likely to be even higher after occlusion of a stent used to treat AMI, because of less well-developed collateral circulation. Emergency stenting for AMI may be performed under inferior radiological conditions compared with elective stenting, and the clinical consequences of a restenosis or re-occlusion are probably more severe.
      Figure thumbnail fx10

      2.6 Medical treatment of mesenteric arterial disease

      Figure thumbnail fx11

      3. Arterial ischaemia, chronic mesenteric ischaemia

      3.1 Symptoms and signs

      CMI is commonly characterised by postprandial abdominal pain, and when severe, food aversion and weight loss. The typical pain is mid-abdominal or epigastric and can be sharp or dull, usually beginning 20–30 minutes after eating and lasting 1–2 hours. The abdominal pain associated with eating causes patients to reduce food intake and this leads to significant weight loss. Patients presenting with a possible diagnosis of CMI without substantial weight loss should be further investigated for an alternative diagnosis, although CMI is possible in the presence of normal weight. The diagnosis of CMI is often delayed as patients undergo extensive investigations for possible malignancy or are classified as having functional abdominal disorders. Atypical symptoms like constant abdominal discomfort, nausea, vomiting, diarrhoea, or constipation occasionally can be present, and may indicate end stage ischaemia, that is a risk of developing bowel gangrene. Clinical history and physical examination may reveal atherosclerotic involvement in other locations.
      • Veenstra R.P.
      • ter Steege R.W.
      • Geelkerken R.H.
      • Huisman A.B.
      • Kolkman J.J.
      The cardiovascular risk profile of atherosclerotic gastrointestinal ischemia is different from other vascular beds.
      • Sana A.
      • van Noord D.
      • Mensink P.B.
      • Kooij S.
      • van Dijk K.
      • Bravenboer B.
      • et al.
      Patients with chronic gastrointestinal ischemia have a higher cardiovascular disease risk and mortality.
      Abdominal examination may reveal an epigastric bruit. Laboratory findings are not specific, but may include anaemia, leukopoenia, electrolyte abnormalities, and hypoalbuminaemia secondary to chronic malnutrition.

      3.2 Anatomy and symptomatology

      The anatomy of the three mesenteric arteries CA, SMA, IMA is discussed in Chapter 1.5. A number of collateral pathways provide arterial supply when one or two of the mesenteric arteries are occluded or significantly stenotic (Fig. 1, page 6). It is assumed that the abundant arterial collateral circulation of the mesenteric tract prevents gastrointestinal ischaemia in single vessel disease. This can be demonstrated by stenosis in a single mesenteric artery often being found in the general population (up to 18%), but the diagnosis of mesenteric ischaemia being very rare.
      • Thomas J.H.
      • Blake K.
      • Pierce G.E.
      • Hermreck A.S.
      • Seigel E.
      The clinical course of asymptomatic mesenteric arterial stenosis.
      • Hansen K.J.
      • Wilson D.B.
      • Craven T.E.
      • Pearce J.D.
      • English W.P.
      • Edwards M.S.
      • et al.
      Mesenteric artery disease in the elderly.
      • Wilson D.B.
      • Mostafavi K.
      • Craven T.E.
      • Ayerdi J.
      • Edwards M.S.
      • Hansen K.J.
      Clinical course of mesenteric artery stenosis in elderly americans.
      Symptoms of mesenteric ischaemia are usually not present until at least two of the three mesenteric arteries are significantly stenosed or occluded. Single vessel atherosclerotic occlusion, however, can occasionally cause symptomatic disease.
      • Mensink P.B.
      • van Petersen A.S.
      • Geelkerken R.H.
      • Otte J.A.
      • Huisman A.B.
      • Kolkman J.J.
      Clinical significance of splanchnic artery stenosis.
      • van Noord D.
      • Kuipers E.J.
      • Mensink P.B.
      Single vessel abdominal arterial disease.
      Figure thumbnail fx12

      3.2.1 Diagnostic imaging

      3.2.1.1 Abdominal X-ray

      Plain abdominal X-ray has no role in the diagnosis of CMI. As patients do not develop bowel necrosis the X-rays are usually normal or show nonspecific findings. Vascular calcification may indicate atherosclerotic disease, which can be a clue to the diagnosis, but a normal examination does not exclude CMI.

      3.2.1.2 Ultrasound

      DUS is most often used as the first screening imaging study to diagnose the presence of significant mesenteric arterial stenosis or occlusion. It may also be used to evaluate open and endovascular interventions. The investigation may be technically challenging and requires a skilled specialist. This technique provides the benefit of dynamic assessment of flow through narrowed arterial segments. In one study, 83% of CAs and 93% of SMAs were visualised on the initial DUS, compared with 100% of CAs and 99% of SMAs visualised on DSA.
      • Moneta G.L.
      • Lee R.W.
      • Yeager R.A.
      • Taylor Jr., L.M.
      • Porter J.M.
      Mesenteric duplex scanning: a blinded prospective study.
      DUS interpretation criteria have been defined in several studies, with somewhat diverging results, partly a result of studying different patient populations. Peak systolic velocity (PSV) and end-diastolic velocity (EDV) can be used to predict significant stenosis of the CA and SMA (Table 3). Comparing DUS evaluation to DSA, a diagnostic accuracy of 85–90% was confirmed for the detection of >70% mesenteric artery stenosis.
      • Zwolak R.M.
      • Fillinger M.F.
      • Walsh D.B.
      • LaBombard F.E.
      • Musson A.
      • Darling C.E.
      • et al.
      Mesenteric and celiac duplex scanning: a validation study.
      Postprandial testing with administration of a test meal can be helpful and provides justification for additional imaging of the mesenteric arteries. Interpretation of flow velocities in the mesenteric vessels should take into account both the respiratory cycle and the presence of stenoses in the “other” vessel.
      • van Petersen A.S.
      • Meerwaldt R.
      • Kolkman J.J.
      • Huisman A.B.
      • van der Palen J.
      • van Bockel J.H.
      • et al.
      The influence of respiration on criteria for transabdominal duplex examination of the splanchnic arteries in patients with suspected chronic splanchnic ischemia.
      • van Petersen A.S.
      • Kolkman J.J.
      • Meerwaldt R.
      • Huisman A.B.
      • van der Palen J.
      • Zeebregts C.J.
      • et al.
      Mesenteric stenosis, collaterals, and compensatory blood flow.
      Table 3Duplex criteria of mesenteric artery stenosis.
      First author

      (publication year)
      SMA PSV

      ≥ 50% stenosis
      SMA PSV

      ≥ 70% stenosis
      CA PSV

      ≥ 50% stenosis
      CA PSV

      ≥ 70% stenosis
      SMA EDV

      ≥ 50% stenosis
      SMA EDV

      ≥ 70% stenosis
      CA EDV

      ≥ 50% stenosis
      CA EDV

      ≥ 70% stenosis
      Moneta 1993
      • Moneta G.L.
      • Lee R.W.
      • Yeager R.A.
      • Taylor Jr., L.M.
      • Porter J.M.
      Mesenteric duplex scanning: a blinded prospective study.


      (n=100)
      275 cm/s

      sens 92%

      spec 96%
      200 cm/s

      sens 87%

      spec 80%
      AbuRahma 2012
      • AbuRahma A.F.
      • Stone P.A.
      • Srivastava M.
      • Dean L.S.
      • Keiffer T.
      • Hass S.M.
      • et al.
      Mesenteric/celiac duplex ultrasound interpretation criteria revisited.


      (n=150)
      295 cm/s

      sens 87%

      spec 89%
      400 cm/s

      sens 72%

      spec 93%
      240 cm/s

      sens 87%

      spec 83%
      320 cm/s

      sens 80%

      spec 89%
      45 cm/s

      sens 79%

      spec 79%
      70 cm/s

      sens 65%

      spec 95%
      40 cm/s

      sens 84%

      spec 48%
      100 cm/s

      sens 58%

      spec 91%
      van Petersen 2013
      • van Petersen A.S.
      • Meerwaldt R.
      • Kolkman J.J.
      • Huisman A.B.
      • van der Palen J.
      • van Bockel J.H.
      • et al.
      The influence of respiration on criteria for transabdominal duplex examination of the splanchnic arteries in patients with suspected chronic splanchnic ischemia.


      (n=324)
      ≥ 220 cm/s

      (expiration)

      sens 84%

      spec 76%

      ≥ 277 cm/s

      (inspiration)

      sens 68%

      spec 93%
      ≥ 268 cm/s

      (expiration)

      sens 75%

      spec 86%

      ≥ 205 cm/s

      (inspiration)

      sens 78%

      spec 84%
      ≥ 268 cm/s

      (expiration)

      sens 66%

      spec 80%

      ≥ 243 cm/s

      (inspiration)

      sens 68%

      spec 71%
      ≥ 280 cm/s

      (expiration)

      sens 66%

      spec 77%

      ≥ 272 cm/s

      (inspiration)

      sens 72%

      spec 77%
      ≥ 62 cm/s

      (expiration)

      sens 75%

      spec 94%

      ≥ 52 cm/s

      (inspiration)

      sens 76%

      spec 93%
      ≥ 101 cm/s

      (expiration)

      sens 74%

      spec 96%

      ≥ 52 cm/s

      (inspiration)

      sens 78%

      spec 93%
      ≥ 64 cm/s

      (expiration)

      sens 78%

      spec 65%

      ≥ 83 cm/s

      (inspiration)

      sens 53%

      spec 81%
      ≥ 57 cm/s

      (expiration)

      sens 83%

      spec 56%

      ≥ 84 cm/s

      (inspiration)

      sens 66%

      spec 81%
      SMA = superior mesenteric artery; CA = coeliac artery; PSV = peak systolic velocity; EDV = end-diastolic velocity; sens = sensitivity; spec = specificity.
      DUS is also useful for intra-operative assessment of open surgical procedures on mesenteric arteries. One single centre study reported an 8% incidence of technical errors using routine intra-operative DUS.
      • Moneta G.L.
      • Lee R.W.
      • Yeager R.A.
      • Taylor Jr., L.M.
      • Porter J.M.
      Mesenteric duplex scanning: a blinded prospective study.
      • Zwolak R.M.
      • Fillinger M.F.
      • Walsh D.B.
      • LaBombard F.E.
      • Musson A.
      • Darling C.E.
      • et al.
      Mesenteric and celiac duplex scanning: a validation study.
      • van Petersen A.S.
      • Meerwaldt R.
      • Kolkman J.J.
      • Huisman A.B.
      • van der Palen J.
      • van Bockel J.H.
      • et al.
      The influence of respiration on criteria for transabdominal duplex examination of the splanchnic arteries in patients with suspected chronic splanchnic ischemia.
      • AbuRahma A.F.
      • Stone P.A.
      • Srivastava M.
      • Dean L.S.
      • Keiffer T.
      • Hass S.M.
      • et al.
      Mesenteric/celiac duplex ultrasound interpretation criteria revisited.
      • Oderich G.S.
      • Panneton J.M.
      • Macedo T.A.
      • Noel A.A.
      • Bower T.C.
      • Lee R.A.
      • et al.
      Intraoperative duplex ultrasound of visceral revascularizations: optimizing technical success and outcome.
      • Schaefer P.J.
      • Pfarr J.
      • Trentmann J.
      • Wulff A.M.
      • Langer C.
      • Siggelkow M.
      • et al.
      Comparison of noninvasive imaging modalities for stenosis grading in mesenteric arteries.
      • Perko M.J.
      • Just S.
      • Schroeder T.V.
      Importance of diastolic velocities in the detection of celiac and mesenteric artery disease by duplex ultrasound.
      • Bowersox J.C.
      • Zwolak R.M.
      • Walsh D.B.
      • Schneider J.R.
      • Musson A.
      • LaBombard F.E.
      • et al.
      Duplex ultrasonography in the diagnosis of celiac and mesenteric artery occlusive disease.
      DUS evaluation following endovascular interventions on visceral arteries may be used as an adjunct to clinical assessment. There is no consensus on velocity measurements that define the presence of high grade mesenteric arterial restenosis following open or endovascular revascularisation, but an increase of PSV or EDV in repeated standardised DUS indicates progressive stenosis of the mesenteric arteries.
      • Hodgkiss-Harlow K.
      Interpretation of visceral duplex scanning: before and after intervention for chronic mesenteric ischemia.
      Most centres use similar criteria to those used for native arterial lesions. In the case of abnormal findings, DSA or CTA of the restenosis may be necessary, DSA having the advantage of permitting pressure measurements.
      Figure thumbnail fx13

      3.2.2 Angiography

      DSA has historically been considered to be the gold standard for the diagnosis of mesenteric occlusive disease. It can provide good quality imaging of the mesenteric vasculature and also demonstrates any collateral circulation. In addition, it has the advantage of allowing endovascular procedures to be performed at the same time as the DSA. On the other hand, DSA is an invasive treatment with potential complications, and it exposes patients to radiation. CTA has replaced DSA as a diagnostic modality and can be used as the diagnostic test for planning endovascular treatment. In some centres, pressure gradient measurement across the lesion with simultaneously placed pressure sensors in the aorta and distal to the occlusive lesion, is an integral part of the endovascular procedure.
      • Dias N.V.
      • Acosta S.
      • Resch T.
      • Sonesson B.
      • Alhadad A.
      • Malina M.
      • et al.
      Mid-term outcome of endovascular revascularization for chronic mesenteric ischaemia.
      • Landis M.S.
      • Rajan D.K.
      • Simons M.E.
      • Hayeems E.B.
      • Kachura J.R.
      • Sniderman K.W.
      Percutaneous management of chronic mesenteric ischemia: outcomes after intervention.
      Severe SMA stenosis is defined by a mean arterial pressure gradient across the lesion of 10 mmHg or more (the aim of stenting is to reduce the mean arterial pressure gradient close to 0 mmHg,
      • Dias N.V.
      • Acosta S.
      • Resch T.
      • Sonesson B.
      • Alhadad A.
      • Malina M.
      • et al.
      Mid-term outcome of endovascular revascularization for chronic mesenteric ischaemia.
      see below).

      3.2.2.1 Computed tomography angiography

      CTA is now the imaging method of choice in CMI. With 3D reformatting, it can provide excellent reconstructions of the mesenteric arteries and has a sensitivity and specificity of 96% and 94%, respectively, for the diagnosis of occlusions.
      • Kirkpatrick I.D.
      • Kroeker M.A.
      • Greenberg H.M.
      Biphasic CT with mesenteric CT angiography in the evaluation of acute mesenteric ischemia: initial experience.
      This imaging technique also allows visualisation of other abdominal organs during the same procedure and therefore helps to exclude other causes of chronic abdominal pain. In addition, CTA allows the identification of calcified plaques. Three-dimensional imaging allows evaluation of the collateral circulation which develops in CMI. The CTA findings of localised narrowing with post-stenotic dilatation and the absence of atherosclerotic plaques can support the diagnosis of MALS.
      • Horton K.M.
      • Talamini M.A.
      • Fishman E.K.
      Median arcuate ligament syndrome: evaluation with CT angiography.

      3.2.2.3 Proof of ischaemia (functional evaluation)

      The presence of vessel stenosis is no proof of actual ischaemia, and the clinical history of CMI has a large overlap with many other disorders including those of the pancreas, gall bladder, stomach, and duodenum, as well as functional disorders. This emphasises the need for a functional test that could actually prove ischaemia and distinguish CMI from other conditions. Most experienced physicians do not hesitate to treat patients with weight loss or severe postprandial complaints in the presence of severe multi-vessel involvement. The far more common patient with single vessel stenosis, however, is a different problem. Most will not have ischaemia, and the numbers of these asymptomatic patients referred will probably increase with the increasing use of imaging for other suspected conditions. The number of reliable diagnostic tests, however, remains very limited.
      Proof of actual CMI can be obtained through five types of investigation:
      • i)
        assessment of tissue ischaemia during endoscopy
      • ii)
        measurement of gastrointestinal blood flow
      • iii)
        measurement of decreased tissue PO2 or increased tissue CO2
      • iv)
        measurement of ischaemia specific biomarkers
      • v)
        laparotomy with histopathology.
      Upper gastrointestinal endoscopy showed no abnormalities in a cohort of 41 CMI patients.
      • Van Noord D.
      • Sana A.
      • Benaron D.A.
      • Pattynama P.M.
      • Verhagen H.J.
      • Hansen B.E.
      • et al.
      Endoscopic visible light spectroscopy: a new, minimally invasive technique to diagnose chronic GI ischemia.
      Histopathological examination of gastroduodenal biopsies had no additional value mainly because the abnormalities are minimal and nonspecific.
      • Van Noord D.
      • Biermann K.
      • Moons L.M.
      • Pattynama P.M.
      • Verhagen H.J.
      • Kuipers E.J.
      • et al.
      Histological changes in patients with chronic upper gastrointestinal ischaemia.
      Measurement of blood flow changes in the mesenteric arteries is not sufficient to prove CMI. The presence or absence of collaterals and variable metabolic demand play a crucial but poorly defined role. It was hypothesised that the cumulative gastrointestinal blood flow, measured in the portal vein (PV) or in the entire hepatic circulation should be diminished after a test meal.
      • Zacho H.D.
      • Abrahamsen J.
      Functional versus radiological assessment of chronic intestinal ischaemia.
      One investigation of six patients with severe multi-vessel CMI suggested that a low basal blood flow, or an increase below 30% after a meal would indicate CMI.
      • Hansen H.J.
      • Engell H.C.
      • Ring-Larsen H.
      • Ranek L.
      Splanchnic blood flow in patients with abdominal angina before and after arterial reconstruction. A proposal for a diagnostic test.
      Only small cases series have been published thereafter, and the technique is rarely used anymore. Measurement of PV blood flow might be a less invasive alternative,
      • Tsukuda T.
      • Ito K.
      • Koike S.
      • Sasaki K.
      • Shimizu A.
      • Fujita T.
      • et al.
      Pre- and postprandial alterations of portal venous flow: evaluation with single breath-hold three-dimensional half-Fourier fast spin-echo MR imaging and a selective inversion recovery tagging pulse.
      but to the GWC's knowledge no subsequent studies have been published.
      Measurement of mucosal blood flow combined with oxygen saturation has been used for decades. Recently, an improved technique, visual light spectroscopy, has become available. In the largest published study of 41 CMI patients (diagnosed by a multi-disciplinary team based on evaluation of symptoms, gastrointestinal tonometry, and abdominal CTA or MRA) a sensitivity of 90% and a specificity of 60% were demonstrated.
      • Van Noord D.
      • Sana A.
      • Benaron D.A.
      • Pattynama P.M.
      • Verhagen H.J.
      • Hansen B.E.
      • et al.
      Endoscopic visible light spectroscopy: a new, minimally invasive technique to diagnose chronic GI ischemia.
      The latter seems insufficiently reliable for patient selection.
      Increased luminal PCO2, known as tonometry, is indicative of mesenteric ischaemia, irrespective of flow or metabolism. This has been firmly established in various animal models using both occlusive and non-occlusive causes.
      • Groeneveld A.B.
      • Kolkman J.J.
      Splanchnic tonometry: a review of physiology, methodology, and clinical applications.
      The luminal PCO2 can be measured using a nasogastric and nasojejunal catheter attached to a specially designed capnograph (Tonocap®) that measures the PCO2 automatically. This PCO2 gradient increased only when blood flow was reduced below 50% of the basal flow and then increased sharply.
      • Knichwitz G.
      • Rotker J.
      • Mollhoff T.
      • Richter K.D.
      • Brussel T.
      Continuous intramucosal PCO2 measurement allows the early detection of intestinal malperfusion.
      • Otte J.A.
      • Oostveen E.
      • Geelkerken R.H.
      • Groeneveld A.B.
      • Kolkman J.J.
      Exercise induces gastric ischemia in healthy volunteers: a tonometry study.
      The increased CO2 stems from locally buffered lactic acid in anaerobic metabolism.
      Tonometry, either as an exercise test or after standard test meals, has good accuracy for diagnosing CMI.
      • Mensink P.B.
      • van Petersen A.S.
      • Geelkerken R.H.
      • Otte J.A.
      • Huisman A.B.
      • Kolkman J.J.
      Clinical significance of splanchnic artery stenosis.
      • Otte J.A.
      • Geelkerken R.H.
      • Oostveen E.
      • Mensink P.B.
      • Huisman A.B.
      • Kolkman J.J.
      Clinical impact of gastric exercise tonometry on diagnosis and management of chronic gastrointestinal ischemia.
      The sensitivity and specificity for diagnosing CMI are 76% and 92% for exercise tonometry and 92% and 77% for 24 hours tonometry.
      • Otte J.A.
      • Geelkerken R.H.
      • Oostveen E.
      • Mensink P.B.
      • Huisman A.B.
      • Kolkman J.J.
      Clinical impact of gastric exercise tonometry on diagnosis and management of chronic gastrointestinal ischemia.
      • Sana A.
      • Vergouwe Y.
      • van Noord D.
      • Moons L.M.
      • Pattynama P.M.
      • Verhagen H.J.
      • et al.
      Radiological imaging and gastrointestinal tonometry add value in diagnosis of chronic gastrointestinal ischemia.
      The drawback of tonometry is that the current technique is complicated, time-consuming, and error-prone. The current manufacturer has stopped production and support of the Tonocap®, although catheters are still available, and it is uncertain if other PCO2 based measurements will become available.
      Availability of serological markers for CMI detection could be a major advantage in diagnosis. Most studies of serological markers in mesenteric ischaemia have been performed in AMI or NOMI patients.
      • Thuijls G.
      • van Wijck K.
      • Grootjans J.
      • Derikx J.P.
      • van Bijnen A.A.
      • Heineman E.
      • et al.
      Early diagnosis of intestinal ischemia using urinary and plasma fatty acid binding proteins.
      • Cudnik M.T.
      • Darbha S.
      • Jones J.
      • Macedo J.
      • Stockton S.W.
      • Hiestand B.C.
      The diagnosis of acute mesenteric ischemia: a systematic review and meta-analysis.
      • Acosta S.
      • Nilsson T.
      Current status on plasma biomarkers for acute mesenteric ischemia.
      • van Wijck K.
      • Lenaerts K.
      • van Loon L.J.
      • Peters W.H.
      • Buurman W.A.
      • Dejong C.H.
      Exercise-induced splanchnic hypoperfusion results in gut dysfunction in healthy men.
      In a pilot study in 24 CMI patients it was demonstrated that ischaemia was associated with I-FABP increase after meals.
      • Mensink P.B.
      • Hol L.
      • Borghuis-Koertshuis N.
      • Geelkerken R.H.
      • Huisman A.B.
      • Doelman C.J.
      • et al.
      Transient postprandial ischemia is associated with increased intestinal fatty acid binding protein in patients with chronic gastrointestinal ischemia.
      No large studies have been published in CMI patients so far, so serology remains an unproven diagnostic tool for the foreseeable future.
      Accurate functional testing is urgently required to help diagnose suspected CMI, in particular in one vessel disease. Currently, however, the methodology is not yet validated and widespread enough to issue any recommendations on its use.

      3.2.3 Treatment

      Revascularisation is indicated in patients who develop symptoms of CMI. There is no role for a conservative approach with long-term chronic parenteral nutrition and non-interventional therapy. In fact, excessive delays in proceeding with definitive revascularisation or use of parenteral nutrition alone have been associated with clinical deterioration, bowel infarction, and risk of sepsis from catheter related complications.
      • Rheudasil J.M.
      • Stewart M.T.
      • Schellack J.V.
      • Smith 3rd, R.B.
      • Salam A.A.
      • Perdue G.D.
      Surgical treatment of chronic mesenteric arterial insufficiency.
      The goals of mesenteric revascularisation include relief of symptoms, improving quality of life, restoration of normal weight, and improving survival by prevention of bowel infarction. Prophylactic revascularisation in patients with asymptomatic disease is controversial and is rarely performed. Based on one report there may be a role for prophylactic revascularisation in patients with severe three vessel disease who have difficult access to medical care or who live in remote or underserved areas.
      • Thomas J.H.
      • Blake K.
      • Pierce G.E.
      • Hermreck A.S.
      • Seigel E.
      The clinical course of asymptomatic mesenteric arterial stenosis.
      If a conservative approach is taken, these patients need to be closely monitored and counselled regarding symptoms of mesenteric ischaemia. A low threshold is recommended for proceeding with revascularisation if the patient develops any gastrointestinal symptoms such as abdominal bloating, diarrhoea, or atypical pain. Mesenteric revascularisation during other concomitant aortic reconstructions also remains controversial because combined reconstructions have higher morbidity and mortality rates.
      The relevance of single vessel mesenteric stenosis is controversial. It has been shown that long-term improvement can be achieved by treatment and therefore the main question is how to select patients who will benefit from treatment. Two reports that have studied this found that clinical history has a low predictive value.
      • Sana A.
      • Vergouwe Y.
      • van Noord D.
      • Moons L.M.
      • Pattynama P.M.
      • Verhagen H.J.
      • et al.
      Radiological imaging and gastrointestinal tonometry add value in diagnosis of chronic gastrointestinal ischemia.
      • ter Steege R.W.
      • Sloterdijk H.S.
      • Geelkerken R.H.
      • Huisman A.B.
      • van der Palen J.
      • Kolkman J.J.
      Splanchnic artery stenosis and abdominal complaints: clinical history is of limited value in detection of gastrointestinal ischemia.
      Comparing the clinical presentation of 109 patients with CMI to 161 patients without ischaemia, only postprandial pain, weight loss, an altered eating pattern, and diarrhoea were of some value. Even when all four symptoms were present, the probability of CMI was only 60%.
      • ter Steege R.W.
      • Sloterdijk H.S.
      • Geelkerken R.H.
      • Huisman A.B.
      • van der Palen J.
      • Kolkman J.J.
      Splanchnic artery stenosis and abdominal complaints: clinical history is of limited value in detection of gastrointestinal ischemia.
      This emphasises the need for functional tests, especially in patients with single vessel disease.
      Figure thumbnail fx15

      3.2.4 Treatment strategies

      Revascularisation strategies to treat CMI continue to evolve with rapid development of novel endovascular devices and techniques. During the last decade the number of mesenteric revascularisations has increased tenfold because of increasing recognition and the advent of endovascular therapy, which allows a less invasive treatment alternative.
      • Schermerhorn M.L.
      • Giles K.A.
      • Hamdan A.D.
      • Wyers M.C.
      • Pomposelli F.B.
      Mesenteric revascularization: management and outcomes in the United States, 1988–2006.
      In most centres angioplasty and stenting have become the primary treatment modalities, relegating open surgical bypass to patients who are not candidates or who fail endovascular therapy.
      • Schermerhorn M.L.
      • Giles K.A.
      • Hamdan A.D.
      • Wyers M.C.
      • Pomposelli F.B.
      Mesenteric revascularization: management and outcomes in the United States, 1988–2006.
      • Oderich G.S.
      • Bower T.C.
      • Sullivan T.M.
      • Bjarnason H.
      • Cha S.
      • Gloviczki P.
      Open versus endovascular revascularization for chronic mesenteric ischemia: risk-stratified outcomes.
      • Oderich G.S.
      • Gloviczki P.
      • Bower T.C.
      Open surgical treatment for chronic mesenteric ischemia in the endovascular era: when it is necessary and what is the preferred technique?.
      In a recent systematic review endovascular revascularisation was demonstrated to have a mortality risk of 6% (range 0–21%).
      • van Petersen A.S.
      • Kolkman J.J.
      • Beuk R.J.
      • Huisman A.B.
      • Doelman C.J.
      • Geelkerken R.H.
      • et al.
      Open or percutaneous revascularization for chronic splanchnic syndrome.
      Compared with open surgical bypass, endovascular revascularisation has been associated with decreased morbidity, length of stay, and convalescent time.
      • Oderich G.S.
      • Bower T.C.
      • Sullivan T.M.
      • Bjarnason H.
      • Cha S.
      • Gloviczki P.
      Open versus endovascular revascularization for chronic mesenteric ischemia: risk-stratified outcomes.
      • van Petersen A.S.
      • Kolkman J.J.
      • Beuk R.J.
      • Huisman A.B.
      • Doelman C.J.
      • Geelkerken R.H.
      • et al.
      Open or percutaneous revascularization for chronic splanchnic syndrome.
      A meta-analysis of mortality following open and endovascular revascularisation has been performed by the GWC (Fig. 5). Although it could be questioned whether an unpublished meta-analysis should be included in a guideline, the GWC thought the issue to be of such great clinical importance that they performed the analysis themselves, using the methodology described in: www.prisma-statement.org. In single centre cohorts, from highly specialised centres, no difference in mortality was identified (OR 1.12, 95% CI 0.6–2.08). In administrative data from the Nationwide Inpatient Sample from the USA, however, the mortality was lower after endovascular revascularisation (OR 0.20, 95% CI 0.17–0.24).
      • Schermerhorn M.L.
      • Giles K.A.
      • Hamdan A.D.
      • Wyers M.C.
      • Pomposelli F.B.
      Mesenteric revascularization: management and outcomes in the United States, 1988–2006.
      • Moghadamyeghaneh Z.
      • Carmichael J.C.
      • Mills S.D.
      • Dolich M.O.
      • Pigazzi A.
      • Fujitani R.M.
      • et al.
      Early outcome of treatment of chronic mesenteric ischemia.
      Figure 5
      Figure 5Meta-analysis of mortality after open and endovascular revascularisation. (This meta-analysis was performed by the GWC in March 2016, and is only published in this document.)
      Figure thumbnail fx16

      3.2.5 Endovascular revascularisation

      The SMA is the main primary target for revascularisation, whenever possible. Revascularisation of the CA or IMA has also been performed, particularly when the SMA is chronically occluded and not suitable for recanalisation. The characteristics of the SMA that affect treatment selection include vessel diameter, extent of stenosis or occlusion, presence of tandem lesions, degree of calcification, and the extent of collateralisation.
      • Moghadamyeghaneh Z.
      • Carmichael J.C.
      • Mills S.D.
      • Dolich M.O.
      • Pigazzi A.
      • Fujitani R.M.
      • et al.
      Early outcome of treatment of chronic mesenteric ischemia.
      • Kasirajan K.
      • O'Hara P.J.
      • Gray B.H.
      • Hertzer N.R.
      • Clair D.G.
      • Greenberg R.K.
      • et al.
      Chronic mesenteric ischemia: open surgery versus percutaneous angioplasty and stenting.
      • Assar A.N.
      • Abilez O.J.
      • Zarins C.K.
      Outcome of open versus endovascular revascularization for chronic mesenteric ischemia: review of comparative studies.
      • Atkins M.D.
      • Kwolek C.J.
      • LaMuraglia G.M.
      • Brewster D.C.
      • Chung T.K.
      • Cambria R.P.
      Surgical revascularization versus endovascular therapy for chronic mesenteric ischemia: a comparative experience.
      Angioplasty and stenting are most effective for relatively short focal SMA stenoses or occlusions with minimal to moderate calcification or thrombus. Endovascular revascularisation also may be possible in patients with longer segment occlusions or excessively calcified vessels.
      • Manunga J.M.
      • Oderich G.S.
      Orbital atherectomy as an adjunct to debulk difficult calcified lesions prior to mesenteric artery stenting.
      • Sarac T.P.
      • Altinel O.
      • Kashyap V.
      • Bena J.
      • Lyden S.
      • Sruvastava S.
      • et al.
      Endovascular treatment of stenotic and occluded visceral arteries for chronic mesenteric ischemia.
      For CA lesions, angioplasty and stenting carries a higher rate of restenosis,
      • Malgor R.D.
      • Oderich G.S.
      • McKusick M.A.
      • Misra S.
      • Kalra M.
      • Duncan A.A.
      • et al.
      Results of single- and two-vessel mesenteric artery stents for chronic mesenteric ischemia.
      and should not be performed if there is active compression by the median arcuate ligament. CA stenting is an option if the vessel is not compressed or if the median arcuate ligament has been surgically released using a laparoscopic or open technique.
      The role of two vessel stenting (of both the CA and the SMA) remains controversial, but most reports indicate that angioplasty and stenting of a single vessel may be sufficient. Two retrospective studies have shown a non-significant trend towards lower recurrence with two vessel stenting,
      • Silva J.A.
      • White C.J.
      • Collins T.J.
      • Jenkins J.S.
      • Andry M.E.
      • Reilly J.P.
      • et al.
      Endovascular therapy for chronic mesenteric ischemia.
      • Peck M.A.
      • Conrad M.F.
      • Kwolek C.J.
      • LaMuraglia G.M.
      • Paruchuri V.
      • Cambria R.P.
      Intermediate-term outcomes of endovascular treatment for symptomatic chronic mesenteric ischemia.
      and another study showed more frequent long-term success after two vessel repair.
      • Groeneveld A.B.
      • Kolkman J.J.
      Splanchnic tonometry: a review of physiology, methodology, and clinical applications.
      On the other hand, another study reported nearly identical recurrence rates at 2 years in patients treated with SMA stents (78%) compared with two vessel stenting of the SMA and CA (60%).
      • Malgor R.D.
      • Oderich G.S.
      • McKusick M.A.
      • Misra S.
      • Kalra M.
      • Duncan A.A.
      • et al.
      Results of single- and two-vessel mesenteric artery stents for chronic mesenteric ischemia.
      Two vessel mesenteric interventions may have a role in selected patients with severe gastric ischaemia who do not have a good collateral network between the CA and SMA. A second intervention adds cost and potential risk of complications, but there are some data indicating that two vessel revascularisation is superior to one vessel revascularisation.
      • Groeneveld A.B.
      • Kolkman J.J.
      Splanchnic tonometry: a review of physiology, methodology, and clinical applications.
      • Atkins M.D.
      • Kwolek C.J.
      • LaMuraglia G.M.
      • Brewster D.C.
      • Chung T.K.
      • Cambria R.P.
      Surgical revascularization versus endovascular therapy for chronic mesenteric ischemia: a comparative experience.
      • Biebl M.
      • Oldenburg W.A.
      • Paz-Fumagalli R.
      • McKinney J.M.
      • Hakaim A.G.
      Surgical and interventional visceral revascularization for the treatment of chronic mesenteric ischemia–when to prefer which?.
      • Gupta P.K.
      • Horan S.M.
      • Turaga K.K.
      • Miller W.J.
      • Pipinos I.I.
      Chronic mesenteric ischemia: endovascular versus open revascularization.
      The GWC did not consider the data robust enough, however, to issue a recommendation to support routine two vessel over one vessel revascularisation.
      CA intervention may be considered in higher risk patients who have had failed recanalisation of the SMA, or in those in whom an SMA intervention is felt to have a low chance of success because of excessive calcification or long segment occlusion. In some patients, coeliac stenting may be considered a “bridge” to open bypass or retrograde SMA stenting.
      • Biebl M.
      • Oldenburg W.A.
      • Paz-Fumagalli R.
      • McKinney J.M.
      • Hakaim A.G.
      Endovascular treatment as a bridge to successful surgical revascularization for chronic mesenteric ischemia.
      Evidence for the efficacy of angioplasty of the IMA is limited, although a case series of four patients with successful results has been reported.
      • Wohlauer M.
      • Kobeiter H.
      • Desgranges P.
      • Becquemin J.P.
      • Cochennec F.
      Inferior mesenteric artery stenting as a novel treatment for chronic mesenteric ischaemia in patients with an occluded superior mesenteric artery and celiac trunk.
      The indication for IMA angioplasty remains unclear.
      In many centres, an endovascular first approach is used, regardless of the patient's clinical risk. Anatomical factors that increase the technical difficulty of endovascular procedures include severe eccentric calcification, flush occlusions, and long lesions that extend into the mid-segment of the SMA. In these cases, stenting may be possible, but the technical result is not optimal and restenosis or intra-procedural complications can occur.
      • Tallarita T.
      • Oderich G.S.
      • Macedo T.A.
      • Gloviczki P.
      • Misra S.
      • Duncan A.A.
      • et al.
      Reinterventions for stent restenosis in patients treated for atherosclerotic mesenteric artery disease.
      • Oderich G.S.
      • Tallarita T.
      • Gloviczki P.
      • Duncan A.A.
      • Kalra M.
      • Misra S.
      • et al.
      Mesenteric artery complications during angioplasty and stent placement for atherosclerotic chronic mesenteric ischemia.
      Figure thumbnail fx17
      Recanalisation with deliberate sub-intimal angioplasty has also been described,
      • Glasby M.J.
      • Bolia A.
      Treatment of chronic mesenteric ischemia by subintimal angioplasty of an occluded superior mesenteric artery.
      but there are no studies comparing results of this with standard intraluminal angioplasty.
      Figure thumbnail fx18

      3.2.6 Open surgery

      Figure thumbnail fx19

      3.2.6.1 Pre-operative evaluation prior to open surgery

      Pre-operative evaluation should assess surgical risk, nutritional status, and anatomical factors that affect the choice of reconstruction. A comprehensive evaluation of cardiac, pulmonary, and renal function is needed, because these procedures are usually required in patients who have multiple comorbidities. This should not delay treatment in patients requiring urgent revascularisation. Routine cardiac catheterisation is unnecessary and cardiac evaluation and peri-operative management are guided by the recommendations of the European Society of Cardiology for patients undergoing major non-cardiac surgery.
      • Kristensen S.D.
      • Knuuti J.
      • Saraste A.
      • Anker S.
      • Bøtker H.E.
      • De Hert S.
      • et al.
      2014 ESC/ESA Guidelines on non-cardiac surgery: cardiovascular assessment and management: the Joint Task Force on non-cardiac surgery: cardiovascular assessment and management of the European Society of Cardiology (ESC) and the European Society of Anaesthesiology (ESA).
      Although nutritional status and smoking cessation are important, time is most important, and revascularisation must not be delayed.

      3.2.7 Open surgical techniques

      Planning open surgical reconstruction of the mesenteric arteries involves selection of the type of incision (transperitoneal vs. retroperitoneal), conduit (vein vs. prosthetic), graft configuration (antegrade vs. retrograde), source of inflow (aortic vs. iliac), and the number of vessels to be reconstructed (single vs. multiple). The type of open reconstruction should be tailored to the anatomy and to the patient's clinical risk assessment.
      • Oderich G.S.
      • Gloviczki P.
      • Bower T.C.
      Open surgical treatment for chronic mesenteric ischemia in the endovascular era: when it is necessary and what is the preferred technique?.
      Patients with less physiological reserve because of advanced age, cachexia, or severe cardiac, pulmonary, and renal dysfunction are not good candidates for supra-coeliac aortic reconstructions, but may be better suited to extra-anatomical reconstructions based on the infrarenal aorta or iliac artery. Alternatively, the technique of retrograde open mesenteric stenting (ROMS) has been used with surgical exposure of the SMA and introduction of the stent retrogradely via direct puncture.
      • Wyers M.C.
      • Powell R.J.
      • Nolan B.W.
      • Cronenwett J.L.
      Retrograde mesenteric stenting during laparotomy for acute occlusive mesenteric ischemia.
      • Milner R.
      • Woo E.Y.
      • Carpenter J.P.
      Superior mesenteric artery angioplasty and stenting via a retrograde approach in a patient with bowel ischemia–a case report.
      • Pisimisis G.T.
      • Oderich G.S.
      Technique of hybrid retrograde superior mesenteric artery stent placement for acute-on-chronic mesenteric ischemia.
      In the largest series published so far, successful ROMS was reported in 14 of 15 cases, with high secondary patency rates.
      • Blauw J.T.
      • Meerwaldt R.
      • Brusse-Keizer M.
      • Kolkman J.J.
      • Gerrits D.
      • Geelkerken R.H.
      • et al.
      Retrograde open mesenteric stenting for acute mesenteric ischemia.

      3.2.7.1 Antegrade bypass

      The distal thoracic or supra-coeliac aorta is often selected as the inflow source if it is spared from severe atherosclerotic disease. The graft configuration may offer a potential haemodynamic advantage, while avoiding the potential risk of graft kinking that can occur with retrograde grafts.
      • Farber M.A.
      • Carlin R.E.
      • Marston W.A.
      • Owens L.V.
      • Burnham S.J.
      • Keagy B.A.
      Distal thoracic aorta as inflow for the treatment of chronic mesenteric ischemia.
      In most reports, two vessel reconstruction of the CA and the SMA is done using a bifurcated polyethylene terephthalate (e.g. Dacron®) graft.
      • Oderich G.S.
      • Bower T.C.
      • Sullivan T.M.
      • Bjarnason H.
      • Cha S.
      • Gloviczki P.
      Open versus endovascular revascularization for chronic mesenteric ischemia: risk-stratified outcomes.
      • Park W.M.
      • Cherry Jr., K.J.
      • Chua H.K.
      • Clark R.C.
      • Jenkins G.
      • Harmsen W.S.
      • et al.
      Current results of open revascularization for chronic mesenteric ischemia: a standard for comparison.

      3.2.7.2 Retrograde bypass

      A retrograde bypass based on the infrarenal aorta, a previous aortic graft, or the iliac arteries may be preferred if the supra-coeliac aorta is diseased or the patient has compromised cardiac or pulmonary function. Most retrograde reconstructions deal with a single vessel, typically the SMA, but reconstruction of the CA or common hepatic artery can also be achieved by tunnelling the graft retroperitoneally or via the transverse mesocolon. The anastomotic site of the graft is determined by the lack of significant calcification. It can be in the distal aorta or the iliac arteries, which has the advantage of avoiding cross-clamping the aorta. As the graft assumes a C-shaped configuration, it is important to avoid graft elongation, angulation, or kinking. It is also important to cover the graft with an omental flap to avoid contact with the intestines. Reports suggest that retrograde grafts perform as well as antegrade grafts.
      • Oderich G.S.
      • Bower T.C.
      • Sullivan T.M.
      • Bjarnason H.
      • Cha S.
      • Gloviczki P.
      Open versus endovascular revascularization for chronic mesenteric ischemia: risk-stratified outcomes.
      • Park W.M.
      • Cherry Jr., K.J.
      • Chua H.K.
      • Clark R.C.
      • Jenkins G.
      • Harmsen W.S.
      • et al.
      Current results of open revascularization for chronic mesenteric ischemia: a standard for comparison.

      3.2.7.3 Retrograde open mesenteric stenting

      The ROMS technique uses a hybrid approach via a midline laparotomy to expose the SMA or CA combined with endovascular retrograde stenting.
      • Wyers M.C.
      • Powell R.J.
      • Nolan B.W.
      • Cronenwett J.L.
      Retrograde mesenteric stenting during laparotomy for acute occlusive mesenteric ischemia.
      • Milner R.
      • Woo E.Y.
      • Carpenter J.P.
      Superior mesenteric artery angioplasty and stenting via a retrograde approach in a patient with bowel ischemia–a case report.
      ROMS is an alternative if percutaneous stenting via the aorta fails. It avoids the need for extensive dissection, vein harvesting, and use of a prosthetic graft, and may be ideal in patients with extensive aorto-iliac disease and no good inflow source, or in those with bowel gangrene and contamination.
      The SMA is dissected out below the pancreas and any jejunal branches are controlled prior to catheter manipulations. Retrograde access is established with a guidewire and sheath. The narrowed or occluded vessel is treated by angioplasty and stenting, most often using a balloon expandable stent. It can sometimes be easier to snare the guidewire in the aorta, and then work from the groin or the arm rather than from the abdomen. The puncture site is closed with interrupted sutures or opened longitudinally and closed with a patch if severely diseased. Re-entry into the aorta can sometimes be difficult with this technique, and there is a risk of causing an aortic dissection.

      3.3 Results and follow-up

      Most publications on the treatment of CMI report 30 day and in hospital outcomes. Those studies that report longer follow-up often have incomplete data and therefore the long-term outcome of mesenteric revascularisation is difficult to assess. Some studies report outcomes until 5 years after treatment, but there is little information beyond this time period.
      A review
      • Assar A.N.
      • Abilez O.J.
      • Zarins C.K.
      Outcome of open versus endovascular revascularization for chronic mesenteric ischemia: review of comparative studies.
      of eight studies (n=247) comparing open versus endovascular revascularisation for CMI identified a higher technical success rate for open compared with endovascular intervention, but for the latter this improved with time. The rate of early post-operative symptom relief (five studies) was higher for open versus endovascular revascularisation, but significantly higher in only two studies (71% vs. 33%, p=.01 and 100% vs. 79%, p=.03). The rate of late symptom relief (seven studies, follow-up 1–3 years) was also higher for open versus endovascular revascularisation, and significantly higher in five studies (range 59–100% for open revascularisation and 22–75% for endovascular revascularisation; p=.0004 to p=.02). There was no significant difference in the 30-day mortality rates. Rates of medium-term restenosis (five studies) and re-intervention (four studies) were reported to be significantly lower for open revascularisation. Primary graft patency was higher for open revascularisation at 6 months (one study), 1 year (one study, 90% vs. 58%, p<.001), and 2 years (one study). Secondary graft patency was higher for open revascularisation at 2 years (two studies; 87% vs. 69%, p=.003 and 100% vs. 65%, p=.006) and 3 years (one study).
      In a retrospective study of 86 open revascularisation procedures performed for CMI, primary outcomes were 30 day mortality and morbidity, and secondary outcomes were survival, primary patency (PP), secondary patency, and freedom from digestive symptoms, depending on the completeness of the revascularisation performed.
      • Schaefer P.J.
      • Schaefer F.K.
      • Mueller-Huelsbeck S.
      • Jahnke T.
      Chronic mesenteric ischemia: stenting of mesenteric arteries.
      Median follow-up was 6.9 years (range 0.3–20.0). The 30 day mortality and morbidity rates were, respectively, 3.5% and 13.9%. Ten year survival was 88% for complete and 76% for incomplete revascularisation (p=.54). The PP was 84% at 10 years for complete and 87% for incomplete revascularisation (p=.51). The 10-year secondary patency was 92% for complete and 93% for incomplete revascularisation (p=.63). Freedom from gastrointestinal symptoms was influenced by the completeness of revascularisation: 79% for complete versus 65% for incomplete revascularisation at 10 years (p=.04).
      The possible benefits of imaging follow-up after mesenteric revascularisation are unknown. If routine imaging (US/CTA/MRA) is performed it is also unknown what management would be recommended if an asymptomatic restenosis was found. In a study of 157 patients treated for CMI by mesenteric artery angioplasty and stenting, 57 patients (36%) developed a restenosis after a mean follow-up of 29 months.
      • Raupach J.
      • Lojik M.
      • Chovanec V.
      • Renc O.
      • Strycek M.
      • Dvorak P.
      • et al.
      Endovascular management of acute embolic occlusion of the superior mesenteric artery: a 12-year single-centre experience.
      Thirty patients underwent treatment, 24 of whom presented with recurrent symptoms and six had pre-occlusive lesions. Mesenteric re-interventions were associated with a low mortality (3%), a high complication rate (27%) (e.g. access site problems, bowel ischaemia, congestive cardiac failure, and stent thrombosis) and excellent symptom improvement (92%). In another report on 24 patients who underwent SMA stenting for CMI and who were followed with DUS, eight re-interventions were performed.
      It follows from examining the data in these and other studies that the main reason to follow patients up after mesenteric revascularisation is to assess restenosis of an angioplasty or stented site or to identify a stenosed or occluded surgical graft. The majority of cases who proceed to treatment in this situation, however, are patients who have recurrent symptoms following previous treatment. There is little evidence therefore to indicate that routine follow-up, either clinically, or with some modality of vascular imaging is of benefit. The European Society of Cardiology guidelines on the treatment of peripheral arterial diseases recommend duplex ultrasound every 6–12 months but again there is no evidence to support this.
      • European Stroke O.
      • Tendera M.
      • Aboyans V.
      • Bartelink M.L.
      • Baumgartner I.
      • Clement D.
      • et al.
      ESC guidelines on the diagnosis and treatment of peripheral artery diseases: document covering atherosclerotic disease of extracranial carotid and vertebral, mesenteric, renal, upper and lower extremity arteries: the Task Force on the Diagnosis and Treatment of Peripheral Artery Diseases of the European Society of Cardiology (ESC).
      When deciding on follow-up (clinical and/or with imaging) the value not only for the patient, but also the competence of the multidisciplinary team investigating and treating patients with CMI, must be considered.
      • Baker A.C.
      • Chew V.
      • Li C.S.
      • Lin T.C.
      • Dawson D.L.
      • Pevec W.C.
      • et al.
      Application of duplex ultrasound imaging in determining in-stent stenosis during surveillance after mesenteric artery revascularization.
      Figure thumbnail fx21
      Figure thumbnail fx22

      4. Arterial ischaemia, non-occlusive mesenteric ischaemia

      4.1 Background and definition

      Acute and chronic arterial occlusions leading to mesenteric ischaemia have been discussed in the previous chapters. Arterial occlusion is not always necessary to produce intestinal gangrene. Ischaemia develops when the oxygen supply to the intestines is insufficient to meet metabolic needs. The term NOMI was first suggested by Ende in 1958.
      • Ende N.
      Infarction of the bowel in cardiac failure.
      In the critically ill patient, often having a low CO, multiple interventions are performed to save the patient's life.
      • Bjorck M.
      • Wanhainen A.
      Nonocclusive mesenteric hypoperfusion syndromes: recognition and treatment.
      In this situation the intestinal circulation may be compromised, sometimes as a side effect of resuscitation causing vasoconstriction of the mesenteric circulation, or caused by an ACS.
      • Kirkpatrick A.W.
      • Roberts D.J.
      • De Waele J.
      • Jaeschke R.
      • Malbrain M.L.
      • De Keulenaer B.
      • et al.
      Intra-abdominal hypertension and the abdominal compartment syndrome: updated consensus definitions and clinical practice guidelines from the World Society of the Abdominal Compartment Syndrome.
      Although the definition may seem rather straightforward, that is there is no occlusion of the mesenteric arteries, it is not easy to define NOMI. The main mechanism underlying NOMI is mesenteric vasoconstriction in response to reduced effective blood volume.
      • Kolkman J.J.
      • Mensink P.B.
      Non-occlusive mesenteric ischaemia: a common disorder in gastroenterology and intensive care.
      NOMI can develop in a patient with asymptomatic mesenteric atherosclerosis, for example when circulatory shock develops in the presence of mesenteric stenosis. This combination may change a previously asymptomatic stenosis of a mesenteric artery into life threatening mesenteric ischaemia if hypotension, hypovolaemia, or ACS develops. It is suggested therefore that NOMI is defined in the following way:NOMI is defined as a hypoperfusion syndrome that occurs when severe ischaemia of the intestines develops, despite the mesenteric arteries being patent. It is caused by either mesenteric vasoconstriction secondary to conditions such as heart failure, vasoconstrictive medication, and hypovolaemia or by increased intra-abdominal pressure.”
      The subgroup of patients who have an underlying arterial stenosis is an important one, as it affects both diagnosis and treatment, to be discussed below. There are a number of clinical scenarios in which NOMI can develop, and the most common are the following:
      • a)
        The patient with severe cardiac failure, needing massive inotropic support or an intra-aortic balloon pump device to survive. Even compensated patients with cardiac failure have been shown to have mild NOMI.
        • Krack A.
        • Richartz B.M.
        • Gastmann A.
        • Greim K.
        • Lotze U.
        • Anker S.D.
        • et al.
        Studies on intragastric PCO2 at rest and during exercise as a marker of intestinal perfusion in patients with chronic heart failure.
      • b)
        In the post-operative period after cardiac surgery.
      • c)
        Intestinal hypoperfusion following renal replacement therapy or massive burn injury, in both situations associated with hypovolemia.
      • d)
        Patients with ACS, in particular after massive bleeding, with or without trauma.
      • e)
        Intestinal hypoperfusion following aortic dissection type A or B.
      • f)
        Colonic ischaemia following AAA repair.
      • g)
        Patients with severe sepsis.
      According to the recently published Management of Descending Thoracic Aorta Diseases Clinical Practice Guidelines (of the ESVS), the risk of developing visceral ischaemia after type B aortic dissection (TBAD) is approximately 7%.
      • Riambau V.
      • Böckler D.
      • Brunkwall J.
      • Cao P.
      • Chiesa R.
      • Coppi G.
      • et al.
      Editor's choice. Management of descending thoracic aorta diseases. Clinical practice guidelines of the European Society for Vascular Surgery.
      That may develop either as systemic hypoperfusion secondary to compression of the true lumen, or as a specific malperfusion of the mesenteric arteries. According to the International Registry of Aortic Dissection, visceral ischaemia is the third most common cause of death in patients with TBAD (after aortic rupture and tamponade).
      • Hagan P.G.
      • Nienaber C.A.
      • Isselbacher E.M.
      • Bruckman D.
      • Karavite D.J.
      • Russman P.L.
      • et al.
      The International Registry of Acute Aortic Dissection (IRAD): new insights into an old disease.
      Given this background, the mentioned guidelines recommend that patients with acute TBAD who develop new or recurrent abdominal pain and, where there is suspicion of visceral, renal, and/or limb malperfusion, should undergo repeat CTA (Class I, Level C).
      • Riambau V.
      • Böckler D.
      • Brunkwall J.
      • Cao P.
      • Chiesa R.
      • Coppi G.
      • et al.
      Editor's choice. Management of descending thoracic aorta diseases. Clinical practice guidelines of the European Society for Vascular Surgery.
      Those guidelines give general recommendations regarding prevention and treatment of malperfusion, and thus are not included in these mesenteric Guidelines.
      Colonic ischaemia is an important complication of AAA repair. The main risk factors are rupture, massive bleeding, and intra-abdominal hypertension or ACS.
      • Bjorck M.
      • Wanhainen A.
      Nonocclusive mesenteric hypoperfusion syndromes: recognition and treatment.
      • Moghadamyeghaneh Z.
      • Carmichael J.C.
      • Mills S.D.
      • Dolich M.O.
      • Pigazzi A.
      • Fujitani R.M.
      • et al.
      Early outcome of treatment of chronic mesenteric ischemia.
      • Djavani K.
      • Wanhainen A.
      • Valtysson J.
      • Bjorck M.
      Colonic ischaemia and intra-abdominal hypertension following open repair of ruptured abdominal aortic aneurysm.
      Although this complication was not covered by the ESVS AAA clinical practice guidelines published in 2011,
      • Moll F.L.
      • Powell J.T.
      • Fraedrich G.
      • Verzini F.
      • Haulon S.
      • Waltham M.
      • et al.
      Management of abdominal aortic aneurysms clinical practice guidelines of the European society for vascular surgery.
      it will be covered by the revised AAA guidelines to be published in 2018. No recommendations are issued on this condition in this document.
      These Guidelines will not discuss further the NOMI associated with severe sepsis, but refer to guidelines focused on intensive care (there are several). There are multiple case reports on the association between use of cocaine or crack cocaine and intestinal ischaemia, affecting different parts of the gastrointestinal tract. It is unclear, however, if this is an occlusive or non-occlusive mechanism, as thrombosis of the SMA has been observed in some cases.
      A special situation occurs if a mesenteric vessel is occluded or stenosed (most often the IMA, but also the SMA or CA) without resulting in any symptoms before the patient develops hypovolaemia and/or hypotension. Is that to be defined as occlusive or non-occlusive disease? This is not crystal clear, and is a grey zone of uncertainty similar to that of acute on chronic mesenteric ischaemia, AMI or CMI?

      4.2 Diagnosis

      In all the clinical scenarios disc