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Abdominal aortic aneurysm follow-up by shear wave elasticity imaging after endovascular repair in a canine model

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Abstract

Objectives

To investigate if shear wave imaging (SWI) can detect endoleaks and characterize thrombus organization in abdominal aortic aneurysms (AAAs) after endovascular aneurysm repair.

Methods

Stent grafts (SGs) were implanted in 18 dogs after surgical creation of type I endoleaks (four AAAs), type II endoleaks (13 AAAs) and no endoleaks (one AAA). Color flow Doppler ultrasonography (DUS) and SWI were performed before SG implantation (baseline), on days 7, 30 and 90 after SG implantation, and on the day of the sacrifice (day 180). Angiography, CT scans and macroscopic tissue sections obtained on day 180 were evaluated for the presence, size and type of endoleaks, and thrombi were characterized as fresh or organized. Endoleak areas in aneurysm sacs were identified on SWI by two readers and compared with their appearance on DUS, CT scans and macroscopic examination. Elasticity moduli were calculated in different regions (endoleaks, and fresh and organized thrombi).

Results

All 17 endoleaks (100 %) were identified by reader 1, whereas 16 of 17 (94 %) were detected by reader 2. Elasticity moduli in endoleaks, and in areas of organized thrombi and fresh thrombi were 0.2 ± 0.4, 90.0 ± 48.2 and 13.6 ± 4.5 kPa, respectively (P < 0.001 between groups). SWI detected endoleaks while DUS (three endoleaks) and CT (one endoleak) did not.

Conclusions

SWI has the potential to detect endoleaks and evaluate thrombus organization based on the measurement of elasticity.

Key points

• SWI has the potential to detect endoleaks in post-EVAR follow-up.

• SWI has the potential to characterize thrombus organization in post-EVAR follow-up.

• SWI may be combined with DUS in post-EVAR surveillance of endoleak.

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Abbreviations

AAA:

Abdominal aortic aneurysm

CEUS:

Contrast-enhanced ultrasonography

CI:

Confidence interval

CT:

Computed tomography

DSA:

Digital subtraction angiography

DUS:

Color flow Doppler ultrasonography

EVAR:

Endovascular repair

MRI:

Magnetic resonance imaging

NIVE:

Non-invasive vascular elastography

ROI:

Region of interest

SG:

Stent graft

SWI:

Shear wave imaging

US:

Ultrasound

References

  1. Eliason JL, Upchurch GR Jr (2009) Endovascular treatment of aortic aneurysms: state of the art. Curr Treat Options Cardiovasc Med 11(2):136–145

    Article  PubMed  Google Scholar 

  2. Zhou W, Blay E Jr, Varu V et al (2014) Outcome and clinical significance of delayed endoleaks after endovascular aneurysm repair. J Vasc Surg 59(4):915–920

    Article  PubMed  Google Scholar 

  3. van Beek SC, Legemate DA, Vahl A et al (2014) External validation of the Endovascular aneurysm repair Risk Assessment model in predicting survival, reinterventions, and endoleaks after endovascular aneurysm repair. J Vasc Surg 59(6):1555–1561.e3

    Article  PubMed  Google Scholar 

  4. Steingruber IE, Neuhauser B, Seiler R et al (2006) Technical and clinical success of infrarenal endovascular abdominal aortic aneurysm repair: a 10-year single-center experience. Eur J Radiol 59(3):384–392

    Article  CAS  PubMed  Google Scholar 

  5. Brown LC, Brown EA, Greenhalgh RM, Powell JT, Thompson SG (2010) Renal function and abdominal aortic aneurysm (AAA): the impact of different management strategies on long-term renal function in the UK EndoVascular Aneurysm Repair (EVAR) Trials. Ann Surg 251(5):966–975

    Article  PubMed  Google Scholar 

  6. Noll RE Jr, Tonnessen BH, Mannava K, Money SR, Sternbergh WC 3rd (2007) Long-term postplacement cost after endovascular aneurysm repair. J Vasc Surg 46(1):9–15, discussion 15

    Article  PubMed  Google Scholar 

  7. White HA, Macdonald S (2010) Estimating risk associated with radiation exposure during follow-up after endovascular aortic repair (EVAR). J Cardiovasc Surg (Torino) 51(1):95–104

    CAS  Google Scholar 

  8. Müller-Wille R, Borgmann T, Wohlgemuth WA et al (2014) Dual-energy computed tomography after endovascular aortic aneurysm repair: the role of hard plaque imaging for endoleak detection. Eur Radiol 24(10):2449–2457

    Article  PubMed  Google Scholar 

  9. AbuRahma AF, Welch CA, Mullins BB, Dyer B (2005) Computed tomography versus color duplex ultrasound for surveillance of abdominal aortic stent-grafts. J Endovasc Ther 12(5):568–573

    Article  PubMed  Google Scholar 

  10. Giannoni MF, Palombo G, Sbarigia E, Speziale F, Zaccaria A, Fiorani P (2003) Contrast-enhanced ultrasound imaging for aortic stent-graft surveillance. J Endovasc Ther 10:208–217

    PubMed  Google Scholar 

  11. Ten Bosch JA, Rouwet EV, Peters CT et al (2010) Contrast-enhanced ultrasound versus computed tomographic angiography for surveillance of endovascular abdominal aortic aneurysm repair. J Vasc Interv Radiol 21(5):638–643

    Article  PubMed  Google Scholar 

  12. Bendick PJ, Zelenock GB, Bove PG, Long GW, Shanley CJ, Brown OW (2003) Duplex ultrasound imaging with an ultrasound contrast agent: the economic alternative to CT angiography for aortic stent graft surveillance. Vasc Endovasc Surg 37:165–170

    Article  Google Scholar 

  13. Karthikesalingam A, Al-Jundi W, Jackson D et al (2012) Systematic review and meta-analysis of duplex ultrasonography, contrast-enhanced ultrasonography or computed tomography for surveillance after endovascular aneurysm repair. Br J Surg 99(11):1514–1523

    Article  CAS  PubMed  Google Scholar 

  14. Abbas A, Hansrani V, Sedgwick N, Ghosh J, McCollum CN (2014) 3D contrast enhanced ultrasound for detecting endoleak following endovascular aneurysm repair (EVAR). Eur J Vasc Endovasc Surg 47(5):487–492

    Article  CAS  PubMed  Google Scholar 

  15. Wilson SR, Greenbaum LD, Goldberg BB (2009) Contrast-enhanced ultrasound: what is the evidence and what are the obstacles? AJR Am J Roentgenol 193:55–60

    Article  PubMed  Google Scholar 

  16. Sarvazyan AP, Rudenko OV, Swanson SD, Fowlkes JB, Emelianov SY (1998) Shear wave elasticity imaging: a new ultrasonic technology of medical diagnostics. Ultrasound Med Biol 24(9):1419–1435

    Article  CAS  PubMed  Google Scholar 

  17. Gürtler VM, Rjosk-Dendorfer D, Reiser M, Clevert DA (2014) Comparison of contrast-enhanced ultrasound and compression elastography in follow-up after endovascular aortic aneurysm repair. Clin Hemorheol Microcirc 57(2):175–183

    PubMed  Google Scholar 

  18. Lerner LS (1996) Modern Physics for Scientists and Engineers, Volume 2. Chapter 22: Summing up. Jones & Bartlett, London, p 622

    Google Scholar 

  19. Canadian Council on Animal Care in Science. Available via http://www.ccac.ca/en_/standards/guidelines. Accessed 30 Jul 2016

  20. National Research Council of the National Academies (2011) Guide for the care and use of laboratory animals. National Academies Press, Washington DC, Available via https://grants.nih.gov/grants/olaw/Guide-for-the-Care-and-use-of-laboratory-animals.pdf. Accessed 30 Jul 2016

    Google Scholar 

  21. Lerouge S, Raymond J, Salazkin I et al (2004) Endovascular aortic aneurysm repair with stent-grafts: experimental models can reproduce endoleaks. J Vasc Interv Radiol 15(9):971–979

    Article  PubMed  Google Scholar 

  22. Soulez G, Lerouge S, Salazkin I, Darsaut T, Oliva VL, Raymond J (2007) Type I and collateral flow in experimental aneurysm models treated with stent-grafts. J Vasc Interv Radiol 18(2):265–272

    Article  PubMed  Google Scholar 

  23. Salloum E, Bertrand-Grenier A, Lerouge S et al (2016) Abdominal aortic aneurysm: follow-up with noninvasive vascular elastography in a canine model. Radiology 279(2):410–419

    Article  PubMed  Google Scholar 

  24. Maurice RL, Ohayon J, Frétigny Y, Bertrand M, Soulez G, Cloutier G (2004) Noninvasive vascular elastography: theoretical framework. IEEE Trans Med Imaging 23(2):164–180

    Article  PubMed  Google Scholar 

  25. Stavropoulos SW, Clark TW, Carpenter JP et al (2005) Use of CT angiography to classify endoleaks after endovascular repair of abdominal aortic aneurysms. J Vasc Interv Radiol 16(5):663–667

    Article  PubMed  Google Scholar 

  26. Cohen J (1960) A coefficient of agreement for nominal scales. Educ Psychol Meas 20(1):37–46

    Article  Google Scholar 

  27. Gürtler VM, Sommer WH, Meimarakis G et al (2013) A comparison between contrast-enhanced ultrasound imaging and multislice computed tomography in detecting and classifying endoleaks in the follow-up after endovascular aneurysm repair. J Vasc Surg 58(2):340–345

    Article  PubMed  Google Scholar 

  28. Perini P, Sediri I, Midulla M, Delsart P, Gautier C, Haulon S (2012) Contrast-enhanced ultrasound vs. CT angiography in fenestrated EVAR surveillance: a single-center comparison. J Endovasc Ther 19(5):648–655

    Article  PubMed  Google Scholar 

  29. Elkouri S, Panneton JM, Andrews JC et al (2004) Computed tomography and ultrasound in follow-up of patients after endovascular repair of abdominal aortic aneurysm. Ann Vasc Surg 18(3):271–279

    Article  PubMed  Google Scholar 

  30. Risberg B, Delle M, Lönn L, Syk I (2004) Management of aneurysm sac hygroma. J Endovasc Ther 11(2):191–195

    Article  PubMed  Google Scholar 

  31. Mfoumou E, Tripette J, Blostein M, Cloutier G (2014) Time-dependent hardening of blood clots quantitatively measured in vivo with shear-wave ultrasound imaging in a rabbit model of venous thrombosis. Thromb Res 133(2):265–271

    Article  CAS  PubMed  Google Scholar 

  32. Kulcsár Z, Houdart E, Bonafé A et al (2011) Intra-aneurysmal thrombosis as a possible cause of delayed aneurysm rupture after flow-diversion treatment. AJNR Am J Neuroradiol 32(1):20–25

    PubMed  Google Scholar 

  33. Ashton JH, Vande Geest JP, Simon BR, Haskett DG (2009) Compressive mechanical properties of the intraluminal thrombus in abdominal aortic aneurysms and fibrin-based thrombus mimics. J Biomech 42(3):197–201

    Article  PubMed  Google Scholar 

  34. Wang DH, Makaroun M, Webster MW, Vorp DA (2001) Mechanical properties and microstructure of intraluminal thrombus from abdominal aortic aneurysm. J Biomech Eng 123(6):536–539

    Article  CAS  PubMed  Google Scholar 

  35. Gasser TC, Görgülü G, Folkesson M, Swedenborg J (2008) Failure properties of intraluminal thrombus in abdominal aortic aneurysm under static and pulsating mechanical loads. J Vasc Surg 48(1):179–188

    Article  PubMed  Google Scholar 

  36. Cornelissen SA, van der Laan MJ, Vincken KL et al (2011) Use of multispectral MRI to monitor aneurysm sac contents after endovascular abdominal aortic aneurysm repair. J Endovasc Ther 18(3):274–279

    Article  PubMed  Google Scholar 

  37. Engellau L, Larsson EM, Albrechtsson U et al (1998) Magnetic resonance imaging and MR angiography of endoluminally treated abdominal aortic aneurysms. Eur J Vasc Endovasc Surg 15(3):212–219

    Article  CAS  PubMed  Google Scholar 

  38. Mori K, Saida T, Sato F et al (2016) Endoleak detection after endovascular aneurysm repair using unenhanced MRI with flow suppression technique: feasibility study in comparison with contrast-enhanced CT. Eur Radiol. doi:10.1007/s00330-016-4315-5

    Google Scholar 

  39. Weigel S, Tombach B, Maintz D et al (2003) Thoracic aortic stent graft: comparison of contrast-enhanced MR angiography and CT angiography in the follow-up: initial results. Eur Radiol 13(7):1628–1634

    Article  PubMed  Google Scholar 

  40. He CM, Roach MR (1994) The composition and mechanical properties of abdominal aortic aneurysms. J Vasc Surg 20(1):6–13

    Article  CAS  PubMed  Google Scholar 

  41. ClinicalTrials.gov (2013) Abdominal aortic aneurysm follow-up after endovascular repair by non-invasive vascular elastography (AAA-Elasto). ClinicalTrials.gov identifier NCT01907386. National Institutes of Health. Available via https://clinicaltrials.gov/ct2/show/NCT01907386?term=abdominal+aortic+aneurysm&recr=Not+yet+recruiting&rslt=Without&type=Intr&titles=abdominal+aortic+aneurysm+followup+after+endovascular+repair+by+noninvasive+vascular+elastography&cntry1=NA%3ACA&state1=NA%3ACA%3AQC&locn=Montreal&rank=1. Accessed 2 Aug 2016

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Acknowledgments

We are grateful to Jocelyn Lavoie, RT, for preparing and organizing the logistics of this project. We thank Michel Gouin, RT, and Gino Potvin, RT, for their work on US and CT acquisition. We also thank the staff of the CRCHUM animal care facility for their expertise in animal experimentation and follow-up.

The scientific guarantor of this publication is Dr. Gilles Soulez, MD, MSc. The authors declare no relationships with any companies, whose products or services may be related to the subject matter of the article. This study received funding by Fonds de Recherche du Québec – Santé (FRQS) (ARQ no. 22951) and the Canadian Institutes of Health Research (MOP no. 115099). G.S. is supported by a National Scientist award from FRQS. A.T. is supported by a Junior 1 Research Award from the FRQS and Fondation de l'association des radiologistes du Québec (no. 26993). Martin Ladouceur, PhD, kindly provided statistical advice. Institutional Review Board approval and written inform consent were not necessary because the study was an animal study. Approval from the institutional animal care committee was obtained. Some study animals or cohorts have been previously reported as part of an investigation of another elastography technique (non-invasive vascular elastography) [23]. The methodology of this project was experimental.

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Authors and Affiliations

  1. Centre de recherche, Centre hospitalier de l’Université de Montréal (CRCHUM), Montréal, Québec, Canada

    Antony Bertrand-Grenier, Sophie Lerouge, An Tang, Eli Salloum, Eric Therasse, Claude Kauffmann, Hélène Héon, Igor Salazkin, Guy Cloutier & Gilles Soulez

  2. Laboratoire de biorhéologie et d’ultrasonographie médicale, CRCHUM, Montréal, Québec, Canada

    Antony Bertrand-Grenier, Eli Salloum & Guy Cloutier

  3. Laboratoire clinique de traitement d’images, CRCHUM, Montréal, Québec, Canada

    Antony Bertrand-Grenier, An Tang, Eli Salloum, Claude Kauffmann & Gilles Soulez

  4. Département de physique, Université de Montréal, Montréal, Québec, Canada

    Antony Bertrand-Grenier

  5. Laboratoire de biomatériaux endovasculaire, CRCHUM, Montréal, Québec, Canada

    Sophie Lerouge

  6. Département de génie mécanique, École de technologie supérieure, Montréal, Québec, Canada

    Sophie Lerouge

  7. Département de radiologie, Centre hospitalier de l’Université de Montréal (CHUM), Montréal, Québec, Canada

    An Tang, Eric Therasse, Claude Kauffmann & Gilles Soulez

  8. Département de radiologie, radio-oncologie et médecine nucléaire, Université de Montréal, Montréal, Québec, Canada

    An Tang, Eric Therasse, Claude Kauffmann, Guy Cloutier & Gilles Soulez

  9. Institut de génie biomédical, Université de Montréal, Montréal, Québec, Canada

    An Tang, Guy Cloutier & Gilles Soulez

Authors
  1. Antony Bertrand-Grenier
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  2. Sophie Lerouge
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  3. An Tang
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  4. Eli Salloum
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  5. Eric Therasse
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  6. Claude Kauffmann
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  7. Hélène Héon
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  8. Igor Salazkin
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  9. Guy Cloutier
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  10. Gilles Soulez
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Corresponding author

Correspondence to Gilles Soulez.

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Bertrand-Grenier, A., Lerouge, S., Tang, A. et al. Abdominal aortic aneurysm follow-up by shear wave elasticity imaging after endovascular repair in a canine model. Eur Radiol 27, 2161–2169 (2017). https://doi.org/10.1007/s00330-016-4524-y

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  • DOI: https://doi.org/10.1007/s00330-016-4524-y

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