Cardiovascular magnetic resonance black-blood thrombus imaging for the diagnosis of acute deep vein thrombosis at 1.5 Tesla

Hanwei Chen, Xueping He, Guoxi Xie, Jianke Liang, Yufeng Ye, Wei Deng, Zhuonan He, Dexiang Liu, Debiao Li, Xin Liu, Zhaoyang Fan, Hanwei Chen, Xueping He, Guoxi Xie, Jianke Liang, Yufeng Ye, Wei Deng, Zhuonan He, Dexiang Liu, Debiao Li, Xin Liu, Zhaoyang Fan

Abstract

Background: The aim was to investigate the feasibility of a cardiovascular magnetic resonance (CMR) black-blood thrombus imaging (BBTI) technique, based on delay alternating with nutation for tailored excitation black-blood preparation and a variable flip angle turbo-spin-echo readout, for the diagnosis of acute deep vein thrombosis (DVT) at 1.5 T.

Methods: BBTI was conducted in 15 healthy subjects and 30 acute DVT patients. Contrast-enhanced CMR venography (CE-CMRV) was conducted for comparison and only performed in the patients. Apparent contrast-to-noise ratios between the thrombus and the muscle/lumen were calculated to determine whether BBTI could provide an adequate thrombus signal for diagnosis. Two blinded readers assessed the randomized BBTI images from all participants and made independent decisions on the presence or absence of thrombus at the segment level. Images obtained by CE-CMRV were also randomized and assessed by the two readers. Using the consensus CE-CMRV as a reference, the sensitivity, specificity, positive and negative predictive values, and accuracy of BBTI, as well as its diagnostic agreement with CE-CMRV, were calculated. Additionally, diagnostic confidence and interobserver diagnostic agreement were evaluated.

Results: The thrombi in the acute phase exhibited iso- or hyperintense signals on the BBTI images. All the healthy subjects were correctly identified from the participants based on the segment level. The diagnostic confidence of BBTI was comparable to that of CE-CMRV (3.69 ± 0.52 vs. 3.70 ± 0.47). High overall sensitivity (95.2%), SP (98.6%), positive predictive value (96.0%), negative predictive value (98.3%), and accuracy (97.7%), as well as excellent diagnostic and interobserver agreements, were achieved using BBTI.

Conclusion: BBTI is a reliable, contrast-free technique for the diagnosis of acute DVT at 1.5 T.

Keywords: Deep vein thrombosis; Magnetic resonance imaging; Venography; Venous thrombosis.

Conflict of interest statement

Ethics approval and consent to participate

This study was approved by the institutional review boards of the Guangzhou Panyu Central Hospital (K20150030 and H20170024). In addition, informed consent was obtained from all the participants.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

Fig. 1
Fig. 1
Representative images obtained by contrast-enhanced cardiovascular magnetic resonance (CE-CMRV) and black blood thrombus imaging (BBTI) from a 55-year-old woman with deep venous thrombosis (DVT) symptom onset at 5 days. The thrombus detected by BBTI showed iso-intense signals within the black-blood venous lumen. The locations and sizes of the thrombi between BBTI and CE-CMRV matched (yellow arrows)
Fig. 2
Fig. 2
Representative images obtained by CE-CMRV and BBTI from a 68-year-old woman with DVT symptom onset at 8 days. The thrombus detected by BBTI showed iso- and hyperintense signals within the black-blood venous lumen. The locations and sizes of the thrombi between BBTI and CE-CMRV matched (yellow arrows)
Fig. 3
Fig. 3
Representative images obtained by CE-CMRV and BBTI from a patient with DVT symptom onset at 10 days. The small thrombus can also be detected by BBTI and matched well with that seen with CE-CMRV (yellow arrows)
Fig. 4
Fig. 4
Results of quantitative signal to noise (SNR) and contrast to noise (CNR) analysis. Both iso−/hyperintense thrombi had adequate signal intensity and contrast to the black-blood venous lumen for the diagnosis of DVT
Fig. 5
Fig. 5
Volume percentage of the iso-intense thrombus in total thrombus volume of each patient. According to the linear regression analysis, the volume percentage of the iso-intense thrombus decreases with the duration of symptoms, indicating that the thrombus signal intensity tends to become stronger
Fig. 6
Fig. 6
Example images obtained in 50-year-old woman with DVT symptom onset at 3 days. The thrombus (green arrows) was detected by BBTI at the asymptomatic right leg, which was missed by the initial ultrasound and confirmed by CE-CMRV. Most parts of the thrombi (yellow arrows) appeared as isointense signals on the BBTI images. The locations and sizes of the thrombi between BBTI and CE-CMRV matched

References

    1. Heit JA, Silverstein MD, Mohr DN, Petterson TM, O'Fallon WM, Melton LJ. Predictors of survival after deep vein thrombosis and pulmonary embolism: a population-based, cohort study. Arch Intern Med. 1999;159:445–453. doi: 10.1001/archinte.159.5.445.
    1. Heit JA. The epidemiology of venous thromboembolism in the community. Arterioscler Thromb Vasc Biol. 2008;28:370–372. doi: 10.1161/ATVBAHA.108.162545.
    1. Beckman MG, Hooper WC, Critchley SE, Ortel TL. Venous thromboembolism: a public health concern. Am J Prev Med. 2010;38:S495–S501. doi: 10.1016/j.amepre.2009.12.017.
    1. Zhang X, Ren Q, Jiang X, Sun J, Gong J, Tang B, et al. A prospective randomized trial of catheter-directed thrombolysis with additional balloon dilatation for iliofemoral deep venous thrombosis: a single-center experience. Cardiovasc Intervent Radiol. 2014;37:958–968. doi: 10.1007/s00270-013-0747-3.
    1. Janssen MC, Wollersheim H, Schultze-Kool LJ, Thien T. Local and systemic thrombolytic therapy for acute deep venous thrombosis. Neth J Med. 2005;63:81–90.
    1. Tan M, Mol GC, van Rooden CJ, Klok FA, Westerbeek RE, del Sol AI, et al. Magnetic resonance direct thrombus imaging differentiates acute recurrent ipsilateral deep vein thrombosis from residual thrombosis. Blood. 2014;124:623–627. doi: 10.1182/blood-2014-04-566380.
    1. Carpenter JP, Holland GA, Baum RA, Owen RS, Carpenter JT, Cope C. Magnetic resonance venography for the detection of deep venous thrombosis: comparison with contrast venography and duplex Doppler ultrasonography. J Vasc Surg. 1993;18:734–741. doi: 10.1016/0741-5214(93)90325-G.
    1. Tan M, van Rooden CJ, Westerbeek RE, Huisman MV. Diagnostic management of clinically suspected acute deep vein thrombosis. Br J Haematol. 2009;146:347–360. doi: 10.1111/j.1365-2141.2009.07732.x.
    1. Goodacre S, Sampson F, Thomas S, van Beek E, Sutton A. Systematic review and meta-analysis of the diagnostic accuracy of ultrasonography for deep vein thrombosis. BMC Med Imaging. 2005;5:6. doi: 10.1186/1471-2342-5-6.
    1. Righini M. Is it worth diagnosing and treating distal deep vein thrombosis? No. J Thromb Haemost. 2007;5:55–59. doi: 10.1111/j.1538-7836.2007.02468.x.
    1. El Kheir D, Büller H. One-time comprehensive ultrasonography to diagnose deep venous thrombosis: is that the solution? Ann Intern Med. 2004;140:1052–1053. doi: 10.7326/0003-4819-140-12-200406150-00016.
    1. Huisman MV, Klok FA. Diagnostic management of acute deep vein thrombosis and pulmonary embolism. J Thromb Haemost. 2013;11:412–422. doi: 10.1111/jth.12124.
    1. Huang SY, Kim CY, Miller MJ, Gupta RT, Lessne ML, Horvath JJ, et al. Abdominopelvic and lower extremity deep venous thrombosis: evaluation with contrast-enhanced MR venography with a blood-pool agent. AJR Am J Roentgenol. 2013;201:208–214. doi: 10.2214/AJR.12.9611.
    1. Ruehm S, Zimny K, Debatin J. Direct contrast-enhanced 3D MR venography. Eur Radiol. 2001;11:102–112. doi: 10.1007/s003300000586.
    1. Sampson FC, Goodacre SW, Thomas SM, van Beek EJ. The accuracy of MRI in diagnosis of suspected deep vein thrombosis: systematic review and meta-analysis. Eur Radiol. 2007;17:175–181. doi: 10.1007/s00330-006-0178-5.
    1. Orbell JH, Smith A, Burnand KG, Waltham M. Imaging of deep vein thrombosis. Br J Surg. 2008;95:137–146. doi: 10.1002/bjs.6077.
    1. Li W, Salanitri J, Tutton S, Dunkle EE, Schneider JR, Caprini JA, et al. Lower extremity deep venous thrombosis: evaluation with ferumoxytol-enhanced MR imaging and dual-contrast mechanism--preliminary experience. Radiology. 2007;242:873–881. doi: 10.1148/radiol.2423052101.
    1. Cantwell CP, Cradock A, Bruzzi J, Fitzpatrick P, Eustace S, Murray JG. MR Venography with true fast imaging with steady-state precession for suspected Lowerlimb deep vein thrombosis. J Vasc Interv Radiol. 2006;17:1763–1770. doi: 10.1097/01.RVI.0000242502.40626.53.
    1. Saha P, Andia ME, Modarai B, Blume U, Humphries J, Patel AS, et al. Magnetic resonance T1 relaxation time of venous thrombus is determined by iron processing and predicts susceptibility to lysis. Circulation. 2013;128:729–736. doi: 10.1161/CIRCULATIONAHA.113.001371.
    1. Moody AR. Direct imaging of deep-vein thrombosis with magnetic resonance imaging. Lancet. 1997;350:1073. doi: 10.1016/S0140-6736(97)24041-9.
    1. Mendichovszky IA, Priest AN, Bowden DJ, Hunter S, Joubert I, Hilborne S, et al. Combined MR direct thrombus imaging and non-contrast magnetic resonance venography reveal the evolution of deep vein thrombosis: a feasibility study. Eur Radiol. 2017;27:2326–2332. doi: 10.1007/s00330-016-4555-4.
    1. Treitl KM, Treitl M, Kooijman-Kurfuerst H, Kammer NN, Coppenrath E, Suderland E, et al. Three-dimensional black-blood T1-weighted turbo spin-echo techniques for the diagnosis of deep vein thrombosis in comparison with contrast-enhanced magnetic resonance imaging: a pilot study. Investig Radiol. 2015;50:401–408. doi: 10.1097/RLI.0000000000000142.
    1. Xie GX, Chen HW, He XP, Liang JK, Deng W, He ZN, et al. Black-blood thrombus imaging (BTI): a contrast-free cardiovascular magnetic resonance approach for the diagnosis of non-acute deep vein thrombosis. J Cardiovasc Magn Reson. 2017;19:4. doi: 10.1186/s12968-016-0320-8.
    1. Kimura K, Iguchi Y, Shibazaki K, Watanabe M, Iwanaga T, Aoki J. M1 susceptibility vessel sign on T2* as a strong predictor for no early recanalization after IV-t-PA in acute ischemic stroke. Stroke. 2009;40:3130–3132. doi: 10.1161/STROKEAHA.109.552588.
    1. Bradley WG., Jr MR appearance of hemorrhage in the brain. Radiology. 1993;189:15–26. doi: 10.1148/radiology.189.1.8372185.
    1. Vedantham S, Grassi CJ, Ferral H, Patel NH, Thorpe PE, Antonacci VP, et al. Reporting standards for endovascular treatment of lower extremity deep vein thrombosis. J Vasc Interv Radiol. 2009;20:S391–S408. doi: 10.1016/j.jvir.2009.04.034.
    1. Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics. 1977;33:159–174. doi: 10.2307/2529310.
    1. Xie Y, Yang Q, Xie G, Pang J, Fan Z, Li D. Improved black-blood imaging using DANTE-SPACE for simultaneous carotid and intracranial vessel wall evaluation. Magn Reson Med. 2016;75:2286–2294. doi: 10.1002/mrm.25785.
    1. Wang J, Helle M, Zhou Z, Bornert P, Hatsukami TS, Yuan C. Joint blood and cerebrospinal fluid suppression for intracranial vessel wall MRI. Magn Reson Med. 2016;75:831–838. doi: 10.1002/mrm.25667.
    1. Li L, Chai JT, Biasiolli L, Robson MD, Choudhury RP, Handa AI, et al. Black-blood multicontrast imaging of carotid arteries with DANTE-prepared 2D and 3D MR imaging. Radiology. 2014;273:560–569. doi: 10.1148/radiol.14131717.
    1. Li L, Miller KL, Jezzard P. DANTE-prepared pulse trains: a novel approach to motion-sensitized and motion-suppressed quantitative magnetic resonance imaging. Magn Reson Med. 2012;68:1423–1438. doi: 10.1002/mrm.24142.
    1. Fraser DG, Moody AR, Morgan PS, Martel AL, Davidson I. Diagnosis of lower-limb deep venous thrombosis: a prospective blinded study of magnetic resonance direct thrombus imaging. Ann Intern Med. 2002;136:89–98. doi: 10.7326/0003-4819-136-2-200201150-00006.
    1. Hulle TVD, Dronkers CEA, Huisman MV, Klok FA. Current standings in diagnostic management of acute venous thromboembolism: still rough around the edges. Blood Rev. 2016;30:21–26. doi: 10.1016/j.blre.2015.07.002.
    1. Aschauer M, Deutschmann HA, Stollberger R, Hausegger KA, Obernosterer A, Schöllnast H, et al. Value of a blood pool contrast agent in MR venography of the lower extremities and pelvis: preliminary results in 12 patients. Magn Reson Med. 2003;50:993–1002. doi: 10.1002/mrm.10607.
    1. Goldhaber SZ, Bounameaux H. Pulmonary embolism and deep vein thrombosis. Lancet. 2012;379:1835–1846. doi: 10.1016/S0140-6736(11)61904-1.
    1. Bates SM, Jaeschke R, Stevens SM, Goodacre S, Wells PS, Stevenson MD, et al. Diagnosis of DVT: antithrombotic therapy and prevention of thrombosis, 9th ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest. 2012;141:e351S–e418S. doi: 10.1378/chest.11-2299.
    1. Blume U, Orbell J, Waltham M, Smith A, Razavi R, Schaeffter T. 3D T 1-mapping for the characterization of deep vein thrombosis. MAGMA. 2009;22:375–383. doi: 10.1007/s10334-009-0189-8.
    1. Evans AJ, Sostman HD, Witty LA, Paulson EK, Spritzer CE, Hertzberg BS, et al. Detection of deep venous thrombosis: prospective comparison of MR imaging and sonography. J Magn Reson Imaging. 1996;6:44–51. doi: 10.1002/jmri.1880060109.
    1. Larsson E-M, Sundén P, Olsson C-G, Debatin Jr, Duerinckx AJ, Baum R, et al. MR venography using an intravascular contrast agent: results from a multicenter phase 2 study of dosage. AJR Am J Roentgenol. 2003;180:227–232. doi: 10.2214/ajr.180.1.1800227.

Source: PubMed

3
Subscribe