Abstract
Objective
This article reviews the relevant anatomy and physiology of the mesenteric vasculature, familiarizes the radiologist with the accepted diagnostic criteria for mesenteric artery stenosis and its role in the diagnosis of chronic mesenteric ischemia, describes Doppler imaging techniques, and provides protocols for the assessment and surveillance of the mesenteric vasculature before and after revascularization. It also discusses expected changes following revascularization and reviews common post-procedural complications.
Results
Duplex sonography plays an important role in the diagnosis and management of chronic mesenteric ischemia (CMI). Establishing a successful diagnosis is dependent upon knowledge of mesenteric arterial anatomy and physiology as well as sufficient expertise in image optimization and scanning techniques. Although there has been a trend toward utilization of other noninvasive [computed tomographic angiography (CTA), magnetic resonance angiography (MRA), and invasive (digital subtraction angiography (DSA)] imaging modalities for assessment of the mesenteric vasculature, a new era of “imaging wisely” raises legitimate concerns about the effects of ionizing radiation as well as potential effects of CT and MR contrast agents. These concerns are obviated by the use of ultrasound, and recently developed techniques, such as contrast-enhanced ultrasound and vascular applications focused on the evaluation of slow flow, have revealed the vast potential of vascular ultrasound in the evaluation of chronic mesenteric ischemia.
Conclusion
Duplex sonography is a cost-effective and powerful tool that can be utilized for the accurate assessment of mesenteric vascular pathology, specifically mesenteric arterial stenosis, and for the evaluation of mesenteric arterial system post revascularization.
Similar content being viewed by others
References
Hansen KJ, Wilson DB, Craven TE, Pearce JD, English WP, Edwards MS, Ayerdi J, Burke GL (2004) Mesenteric artery disease in the elderly. J Vasc Surg 40 (1):45-52. https://doi.org/10.1016/j.jvs.2004.03.022
Hohenwalter EJ (2009) Chronic mesenteric ischemia: diagnosis and treatment. Semin Intervent Radiol 26 (4):345-351. https://doi.org/10.1055/s-0029-1242198
Zeller T, Rastan A, Sixt S (2010) Chronic atherosclerotic mesenteric ischemia (CMI). Vasc Med 15 (4):333-338. https://doi.org/10.1177/1358863X10372437
Cunningham CG, Reilly LM, Stoney R (1992) Chronic visceral ischemia. Surg Clin North Am 72 (1):231-244
Ruzicka FF, Jr., Rossi P (1970) Normal vascular anatomy of the abdominal viscera. Radiol Clin North Am 8 (1):3-29
Kornblith PL, Boley SJ, Whitehouse BS (1992) Anatomy of the splanchnic circulation. Surg Clin North Am 72 (1):1-30
Michels NA (1966) Newer anatomy of the liver and its variant blood supply and collateral circulation. Am J Surg 112 (3):337-347
Wilson DB, Mostafavi K, Craven TE, Ayerdi J, Edwards MS, Hansen KJ (2006) Clinical course of mesenteric artery stenosis in elderly americans. Arch Intern Med 166 (19):2095-2100. https://doi.org/10.1001/archinte.166.19.2095
Lin PH, Chaikof EL (2000) Embryology, anatomy, and surgical exposure of the great abdominal vessels. Surg Clin North Am 80 (1):417-433, xiv
ter Steege RW, Sloterdijk HS, Geelkerken RH, Huisman AB, van der Palen J, Kolkman JJ (2012) Splanchnic artery stenosis and abdominal complaints: clinical history is of limited value in detection of gastrointestinal ischemia. World J Surg 36 (4):793-799. https://doi.org/10.1007/s00268-012-1485-4
Chang JB, Stein TA (2003) Mesenteric ischemia: acute and chronic. Ann Vasc Surg 17 (3):323-328. https://doi.org/10.1007/s10016-001-0249-7
Cognet F, Ben Salem D, Dranssart M, Cercueil JP, Weiller M, Tatou E, Boyer L, Krause D (2002) Chronic mesenteric ischemia: imaging and percutaneous treatment. Radiographics 22 (4):863-879; discussion 879-880. https://doi.org/10.1148/radiographics.22.4.g02jl07863
Moawad J, Gewertz BL (1997) Chronic mesenteric ischemia. Clinical presentation and diagnosis. Surg Clin North Am 77 (2):357-369
Silva JA, White CJ, Collins TJ, Jenkins JS, Andry ME, Reilly JP, Ramee SR (2006) Endovascular therapy for chronic mesenteric ischemia. J Am Coll Cardiol 47 (5):944-950. https://doi.org/10.1016/j.jacc.2005.10.056
Silva JA, White CJ, Collins TJ, Jenkins JS, Andry ME, Reilly JP, Ramee SR (2006) Endovascular therapy for chronic mesenteric ischemia. J Am Coll Cardiol 47 (5):944-950. https://doi.org/10.1016/j.jacc.2005.10.056
Oliva IB, Davarpanah AH, Rybicki FJ, Desjardins B, Flamm SD, Francois CJ, Gerhard-Herman MD, Kalva SP, Ashraf Mansour M, Mohler ER, 3rd, Schenker MP, Weiss C, Dill KE (2013) ACR Appropriateness Criteria (R) imaging of mesenteric ischemia. Abdom Imaging 38 (4):714-719. https://doi.org/10.1007/s00261-012-9975-2
Aburahma AF, Mousa AY, Stone PA, Hass SM, Dean LS, Keiffer T (2012) Duplex velocity criteria for native celiac/superior mesenteric artery stenosis vs in-stent stenosis. J Vasc Surg 55 (3):730-738. https://doi.org/10.1016/j.jvs.2011.10.086
Aburahma AF, Mousa AY, Stone PA, Hass SM, Dean LS, Keiffer T (2012) Duplex velocity criteria for native celiac/superior mesenteric artery stenosis vs in-stent stenosis. J Vasc Surg 55 (3):730-738. https://doi.org/10.1016/j.jvs.2011.10.086
Nicoloff AD, Williamson WK, Moneta GL, Taylor LM, Porter JM (1997) Duplex ultrasonography in evaluation of splanchnic artery stenosis. Surg Clin North Am 77 (2):339-355
Farghadani M, Momeni M, Hekmatnia A, Momeni F, Baradaran Mahdavi MM (2016) Anatomical variation of celiac axis, superior mesenteric artery, and hepatic artery: Evaluation with multidetector computed tomography angiography. J Res Med Sci 21:129. https://doi.org/10.4103/1735-1995.196611
De Martino RR (2015) Normal and Variant Mesenteric Anatomy. In: Oderich GS (ed) Mesenteric vascular disease: current therapy. Springer, New York, pp xviii, 468 pages
Horton KM, Fishman EK (2002) Volume-rendered 3D CT of the mesenteric vasculature: normal anatomy, anatomic variants, and pathologic conditions. Radiographics 22 (1):161-172. https://doi.org/10.1148/radiographics.22.1.g02ja30161
Peripheral Vasculature: Average Vessel Diameter (2015). Boston Scientific Company, Marlborough, MA
Michels NA, Siddharth P, Kornblith PL, Parke WW (1968) Routes of collateral circulation of the gastrointestinal tract as ascertained in a idssection of 500 bodies. Int Surg 49 (1):8-28
Pellerito JS, Revzin MV, Tsang JC, Greben CR, Naidich JB (2009) Doppler sonographic criteria for the diagnosis of inferior mesenteric artery stenosis. J Ultrasound Med 28 (5):641-650
Van Bel F, Van Zwieten PH, Guit GL, Schipper J (1990) Superior mesenteric artery blood flow velocity and estimated volume flow: duplex Doppler US study of preterm and term neonates. Radiology 174 (1):165-169. https://doi.org/10.1148/radiology.174.1.2403678
Parks DA, Jacobson ED (1985) Physiology of the splanchnic circulation. Arch Intern Med 145 (7):1278-1281
Granger DN, Richardson PD, Kvietys PR, Mortillaro NA (1980) Intestinal blood flow. Gastroenterology 78 (4):837-863
Gentile AT, Moneta GL, Lee RW, Masser PA, Taylor LM, Jr., Porter JM (1995) Usefulness of fasting and postprandial duplex ultrasound examinations for predicting high-grade superior mesenteric artery stenosis. Am J Surg 169 (5):476-479. https://doi.org/10.1016/S0002-9610(99)80198-6
van Petersen AS, Meerwaldt R, Kolkman JJ, Huisman AB, van der Palen J, van Bockel JH, Zeebregts CJ, Geelkerken RH (2013) The influence of respiration on criteria for transabdominal duplex examination of the splanchnic arteries in patients with suspected chronic splanchnic ischemia. J Vasc Surg 57 (6):1603-1611, 1611 e1601-1610. https://doi.org/10.1016/j.jvs.2012.11.120
Barr RG (2017) How to Develop a Contrast-Enhanced Ultrasound Program. J Ultrasound Med 36 (6):1225-1240. https://doi.org/10.7863/ultra.16.09045
Blebea J, Volteas N, Neumyer M, Ingraham J, Dawson K, Assadnia S, Anderson KM, Atnip RG (2002) Contrast enhanced duplex ultrasound imaging of the mesenteric arteries. Ann Vasc Surg 16 (1):77-83. https://doi.org/10.1007/s10016-001-0144-2
Rafailidis V, Fang C, Yusuf GT, Huang DY, Sidhu PS (2018) Contrast-enhanced ultrasound (CEUS) of the abdominal vasculature. Abdom Radiol (NY) 43 (4):934-947. https://doi.org/10.1007/s00261-017-1329-7
Piscaglia F, Nolsoe C, Dietrich CF, Cosgrove DO, Gilja OH, Bachmann Nielsen M, Albrecht T, Barozzi L, Bertolotto M, Catalano O, Claudon M, Clevert DA, Correas JM, D’Onofrio M, Drudi FM, Eyding J, Giovannini M, Hocke M, Ignee A, Jung EM, Klauser AS, Lassau N, Leen E, Mathis G, Saftoiu A, Seidel G, Sidhu PS, ter Haar G, Timmerman D, Weskott HP (2012) The EFSUMB Guidelines and Recommendations on the Clinical Practice of Contrast Enhanced Ultrasound (CEUS): update 2011 on non-hepatic applications. Ultraschall Med 33 (1):33-59. https://doi.org/10.1055/s-0031-1281676
Revzin MV, Imanzadeh A, Menias C, Pourjabbar S, Mustafa A, Nezami N, Spektor M, Pellerito JS (2019) Optimizing image quality when evaluating blood flow at Doppler US: a tutorial. Radiographics. https://doi.org/10.1148/rg.2019180055
Jager K, Bollinger A, Valli C, Ammann R (1986) Measurement of mesenteric blood flow by duplex scanning. J Vasc Surg 3 (3):462-469
Moneta GL, Yeager RA, Dalman R, Antonovic R, Hall LD, Porter JM (1991) Duplex ultrasound criteria for diagnosis of splanchnic artery stenosis or occlusion. J Vasc Surg 14 (4):511-518; discussion 518-520
Moneta GL, Lee RW, Yeager RA, Taylor LM, Jr., Porter JM (1993) Mesenteric duplex scanning: a blinded prospective study. J Vasc Surg 17 (1):79-84; discussion 85-76
Lim HK, Lee WJ, Kim SH, Lee SJ, Choi SH, Park HS, Do YS, Choo SW, Choo IW (1999) Splanchnic arterial stenosis or occlusion: diagnosis at Doppler US. Radiology 211 (2):405-410. https://doi.org/10.1148/radiology.211.2.r99ma27405
Bowersox JC, Zwolak RM, Walsh DB, Schneider JR, Musson A, LaBombard FE, Cronenwett JL (1991) Duplex ultrasonography in the diagnosis of celiac and mesenteric artery occlusive disease. J Vasc Surg 14 (6):780-786; discussion 786-788. https://doi.org/10.1067/mva.1991.33215
AbuRahma AF, Stone PA, Srivastava M, Dean LS, Keiffer T, Hass SM, Mousa AY (2012) Mesenteric/celiac duplex ultrasound interpretation criteria revisited. J Vasc Surg 55 (2):428-436 e426; discussion 435-426. https://doi.org/10.1016/j.jvs.2011.08.052
AbuRahma AF, Scott Dean L (2012) Duplex ultrasound interpretation criteria for inferior mesenteric arteries. Vascular 20 (3):145-149. https://doi.org/10.1258/vasc.2011.oa0349
Mirk P (1996) Sonographic and Doppler assessment of the inferior mesenteric artery. J Ultrasound Med 15 (1):78-80
Denys AL, Lafortune M, Aubin B, Burke M, Breton G (1995) Doppler sonography of the inferior mesenteric artery: a preliminary study. J Ultrasound Med 14 (6):435-439; quiz 441-432
Healy DA, Neumyer MM, Atnip RG, Thiele BL (1992) Evaluation of celiac and mesenteric vascular disease with duplex ultrasonography. J Ultrasound Med 11 (9):481-485
Revzin MV (2014) Ultrasonography Assessment of the Aorota and Mesenteric Arterties. In: Chong W (ed) Ultrasound Clinic. Abdominal Ultrasound. Elsevier, pp 723-749
Revzin MV (2013) Ultrasound Assessment of the Splanchnic (Mesenteric) Arteries. In: Pellerito JD (ed) Introduction to Vascular Ultrasonography. 6 edn. Elsevier, pp 517-540
Rizzo RJ, Sandager G, Astleford P, Payne K, Peterson-Kennedy L, Flinn WR, Yao JS (1990) Mesenteric flow velocity variations as a function of angle of insonation. J Vasc Surg 11 (5):688-694
Meyers MA (1976) Griffiths’ point: critical anastomosis at the splenic flexure. Significance in ischemia of the colon. AJR Am J Roentgenol 126 (1):77-94. https://doi.org/10.2214/ajr.126.1.77
Fisher DF, Jr., Fry WJ (1987) Collateral mesenteric circulation. Surg Gynecol Obstet 164 (5):487-492
Yamamoto M, Itamoto T, Oshita A, Matsugu Y (2018) Celiac axis stenosis due to median arcuate ligament compression in a patient who underwent pancreatoduodenectomy; intraoperative assessment of hepatic arterial flow using Doppler ultrasonography: a case report. J Med Case Rep 12 (1):92. https://doi.org/10.1186/s13256-018-1614-2
Akan D, Ozel A, Orhan O, Bozdag E, Basak M (2015) Doppler ultrasound diagnosis of an unusual variant of median arcuate ligament syndrome: concomitant involvement of celiac and superior mesenteric arteries. A case report. Med Ultrason 17 (4):557-560. https://doi.org/10.11152/mu.2013.2066.174.ppd
Aschenbach R, Basche S, Vogl TJ (2011) Compression of the celiac trunk caused by median arcuate ligament in children and adolescent subjects: evaluation with contrast-enhanced MR angiography and comparison with Doppler US evaluation. J Vasc Interv Radiol 22 (4):556-561. https://doi.org/10.1016/j.jvir.2010.11.007
Kim EN, Lamb K, Relles D, Moudgill N, DiMuzio PJ, Eisenberg JA (2016) Median Arcuate Ligament Syndrome-Review of This Rare Disease. JAMA Surg 151 (5):471-477. https://doi.org/10.1001/jamasurg.2016.0002
Gruber H, Loizides A, Peer S, Gruber I (2012) Ultrasound of the median arcuate ligament syndrome: a new approach to diagnosis. Med Ultrason 14 (1):5-9
Pecoraro F, Rancic Z, Lachat M, Mayer D, Amann-Vesti B, Pfammatter T, Bajardi G, Veith FJ (2013) Chronic mesenteric ischemia: critical review and guidelines for management. Ann Vasc Surg 27 (1):113-122. https://doi.org/10.1016/j.avsg.2012.05.012
Zeller T, Macharzina R (2011) Management of chronic atherosclerotic mesenteric ischemia. Vasa 40 (2):99-107. https://doi.org/10.1024/0301-1526/a000079
Malgor RD, Oderich GS, McKusick MA, Misra S, Kalra M, Duncan AA, Bower TC, Gloviczki P (2010) Results of single- and two-vessel mesenteric artery stents for chronic mesenteric ischemia. Ann Vasc Surg 24 (8):1094-1101. https://doi.org/10.1016/j.avsg.2010.07.001
Oderich GS, Tallarita T, Gloviczki P, Duncan AA, Kalra M, Misra S, Cha S, Bower TC (2012) Mesenteric artery complications during angioplasty and stent placement for atherosclerotic chronic mesenteric ischemia. J Vasc Surg 55 (4):1063-1071. https://doi.org/10.1016/j.jvs.2011.10.122
van Petersen AS, Kolkman JJ, Beuk RJ, Huisman AB, Doelman CJ, Geelkerken RH, Multidisciplinary Study Group Of Splanchnic I (2010) Open or percutaneous revascularization for chronic splanchnic syndrome. J Vasc Surg 51 (5):1309-1316. https://doi.org/10.1016/j.jvs.2009.12.064
Armstrong PA (2007) Visceral duplex scanning: evaluation before and after artery intervention for chronic mesenteric ischemia. Perspect Vasc Surg Endovasc Ther 19 (4):386-392; discussion 393-384. https://doi.org/10.1177/1531003507311802
Baker AC, Chew V, Li CS, Lin TC, Dawson DL, Pevec WC, Hedayati N (2012) Application of duplex ultrasound imaging in determining in-stent stenosis during surveillance after mesenteric artery revascularization. J Vasc Surg 56 (5):1364-1371; discussion 1371. https://doi.org/10.1016/j.jvs.2012.03.283
Acknowledgements
The authors thank Henry Douglas for their help with images, Lei Wang for his help with video-recording, Alexandria Brackett for the assistance with literature searches, Melody Polio, Victoria Clifford, Crystal Piper, and Jennifer Smith for their help with obtaining images, and Mary Jo Smallwood for her help in education on new ultrasound vascular platforms.
Funding
None.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Movie 1. The celiac artery landmark.
The celiac artery is best recognized in short axis, where is has a characteristic “seagull sign” or T-shaped appearance that describes the bifurcation of the main celiac artery into the common hepatic artery and splenic artery (MP4 2619 kb)
Movie 2 The SMA landmarks.
The SMA can be quickly identified by scanning in the transverse plane via an anterior epigastric approach. The SMA lies just posterior to the splenic vein, anterior to the left renal vein and the abdominal aorta, and to the right of the SMV. It is surrounded by retroperitoneal fat that is seen on ultrasound as an “echogenic halo sign” (red arrows) (MP4 6671 kb)
Movie 3. IMA Landmarks.
The IMA originates from the left anterolateral aspect of the abdominal aorta and can be seen either on gray-scale imaging (red arrow) or on color Doppler (yellow arrow). It can be either identified on transverse and sagittal planes. On color Doppler blood flow in IMA is demonstrated moving away from the transducer due to the caudad course of the artery toward the left colon, and is thus assigned a blue color (arrow) (MP4 8938 kb)
Movie 4. Grays scale evaluation of the mesenteric arteries.
The mesenteric Doppler examination is preferentially performed in the fasting state. Patients are examined in the supine position, utilizing an anterior epigastric approach that helps to visualize the origins of the mesenteric arteries. Gradual compression technique usually helps to improve visualization of the vasculature by displacing bowel gas away from the transducer . B-mode or gray-scale imaging is imperative in the initial evaluation of the aorta and the mesenteric arteries. Atherosclerotic plaque burden, the presence of a dissection flap, vascular wall thickening, and the presence of either abdominal aortic or mesenteric aneurysm or pseudoaneurysm can all be accurately identified on gray-scale imaging (MP4 12,550 kb)
Movie 5. Color Doppler Evaluation of the mesenteric arteries.
The color Doppler mode aids in determination of vessel patency, flow disturbance and flow direction, and provides average estimation of blood velocity. The identification of disturbed flow on color Doppler, represented by color aliasing, may signify the presence of luminal narrowing or a flow-limiting lesion. Color Doppler images should be initially optimized for laminar flow in the abdominal aorta by adjusting the velocity scale, gain, and wall filter. This aids in detection of abnormalities within the arteries Color Doppler serves as a road map for placement of the spectral gate within an area of abnormality when acquiring quantitative estimation of blood velocity (MP4 14,234 kb)
Movie 6 SMA stenosis and aliasing.
Cine clip through the celiac and mesenteric artery obtained in sagittal plane demonstrates color aliasing at the focal site of narrowing within the SMA (green arrow). Spectral Doppler interrogation obtained at a later time showed high peak systolic velocity at the area of aliasing (not shown) (MP4 7241 kb)
Movie 7. Spectral Doppler evaluation of the mesenteric arteries.
Spectral Doppler mode allows quantitative and qualitative assessment of vascular hemodynamics via calculation of peak systolic velocities throughout the mesenteric arteries, and also via analysis of the waveform pattern. Peak systolic velocities are obtained with mesenteric arteries and the aorta positioned in sagittal plane, using epigastric approach as an acoustic window. Attention is made to the size of the mesenteric arteries, and the size of the aorta at the level of the mesenteric arteries origin. Any areas of narrowing or widening should be interrogated. Peak systolic velocities are performed by placement of the spectral gate in the center of a vessel. Optimization of parameters such as velocity scale, gain and angle correction are important for accurate estimation of the velocities. Preferable angle of insonation should be 60 degrees or less. Manual angle correction can be used to achieve more optimal angles. After obtaining waveforms and velocities at the origin of a mesenteric artery, the cursor is then moved to its proximal, mid and distal segments. Each mesenteric artery is assessed sequentially in the same order, including celiac, superior and inferior mesenteric arteries. In a case of a visible flow disturbance on color Doppler, the area of interest should be careful interrogated with spectral Doppler. The waveform pattern should be analyzed with respect to the presence of a brisk or delayed upstroke and the presence or absence of diastolic flow. An assessment should be also made in regards to flow direction and the presence of collateral vessels. Peak systolic velocities in the celiac artery should be obtained on both inspiration and expiration. Mesenteric-to-aortic PSV ratio is calculated for each mesenteric artery and should be stated in the study report (MP4 14,972 kb)
Rights and permissions
About this article
Cite this article
Revzin, M.V., Pellerito, J.S., Nezami, N. et al. The radiologist’s guide to duplex ultrasound assessment of chronic mesenteric ischemia. Abdom Radiol 45, 2960–2979 (2020). https://doi.org/10.1007/s00261-019-02165-2
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00261-019-02165-2