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CC BY-NC-ND 4.0 · Thromb Haemost 2020; 120(10): 1463-1473
DOI: 10.1055/s-0040-1714280
Stroke, Systemic or Venous Thromboembolism

High Signal Intensity on Diffusion-Weighted Images Reflects Acute Phase of Deep Vein Thrombus

Toshihiro Gi
1   Department of Pathology, Faculty of Medicine, University of Miyazaki, Miyazaki, Japan
,
Yasuyoshi Kuroiwa
1   Department of Pathology, Faculty of Medicine, University of Miyazaki, Miyazaki, Japan
2   Department of Radiological Technology, Koga General Hospital, Miyazaki, Japan
,
Atsushi Yamashita
1   Department of Pathology, Faculty of Medicine, University of Miyazaki, Miyazaki, Japan
,
Yuko Mizutani
3   Division of Radiology, Department of Veterinary Sciences, Faculty of Agriculture, University of Miyazaki, Miyazaki, Japan
,
Taketoshi Asanuma
4   Development of Veterinary Medicine, Faculty of Veterinary Medicine, Imabari Campus, Okayama University of Science, Imabari, Japan
,
Tosiaki Miyati
5   Institute of Medical, Pharmaceutical and Health Sciences, Faculty of Health Sciences, Kanazawa University, Ishikawa, Japan
,
Kazunari Maekawa
1   Department of Pathology, Faculty of Medicine, University of Miyazaki, Miyazaki, Japan
,
Murasaki Aman
6   Department of Diagnostic Pathology, University of Miyazaki Hospital, Faculty of Medicine, University of Miyazaki, Miyazaki, Japan
,
Takuroh Imamura
7   Department of Internal Medicine, Koga General Hospital, Miyazaki, Japan
,
Yujiro Asada
1   Department of Pathology, Faculty of Medicine, University of Miyazaki, Miyazaki, Japan
› Author Affiliations Funding This study was partly supported by Grants-in-Aid for Scientific Research (Nos. JP15K09963, JP16K09019, JP18K15083, JP19K07437, JP19H03445, JP20K08085) from Japan Society for the Promotion of Science, the President's Strategic Priority Budget from Miyazaki University, Clinical Research from Miyazaki University Hospital, and a Research Promotion Grant from The Japanese Society on Thrombosis and Hemostasis.
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Abstract

The effects of antithrombotic therapy on deep vein thrombosis (DVT) can be affected by thrombus age, which cannot be reliably determined by noninvasive imaging modalities. We investigated whether magnetic resonance (MR) diffusion-weighted imaging (DWI) can localize and determine the age of venous thrombus in patients with DVT, animal models, and human blood in vitro. Signal intensity (SI) on DWI and the apparent diffusion coefficient (ADC) of thrombi were assessed in eight patients with DVT using a 1.5-T MR imaging (MRI) system. We assessed the organizing processes as venous thrombus developed in the rabbit jugular vein using a 3.0-T MRI system over time. We also assessed MRI signals of human blood in vitro using the 1.5-T MRI system. Venous thrombi were detected by DWI as areas of high or mixed high and iso SI in all patients. The ADCs were lower in the proximal, than in the distal portion of the thrombi. The thrombi of rabbit jugular veins histologically organized in a time-dependent manner, with high SI on DWI at 4 hours, mixed high and iso SI at 1 and 2 weeks, and iso SI at 3 weeks. The ADC correlated negatively with erythrocyte content, and positively with smooth muscle cells, macrophages, hemosiderin, and collagen content. MRI signals of human blood in vitro showed that ADCs were affected by erythrocyte content, but not by blood clotting. MR-DWI can detect venous thrombus, and high SI on DWI accompanied by a low ADC might reflect erythrocyte-rich, acute-phase thrombi.

Keywords

deep vein thrombosis - diffusion-weighted imaging - erythrocyte - magnetic resonance imaging - pathology

Supplementary Material



Publication History

Received: 10 April 2020

Accepted: 10 June 2020

Article published online:
03 August 2020

© 2020. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial-License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commercial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/).

Georg Thieme Verlag KG
Stuttgart · New York

 

  • References

  • 1 Furukoji E, Gi T, Yamashita A. , et al. CD163 macrophage and erythrocyte contents in aspirated deep vein thrombus are associated with the time after onset: a pilot study. Thromb J 2016; 14: 46
    CrossrefPubMedGoogle Scholar
  • 2 Marder VJ, Sherry S. Thrombolytic therapy: current status (2). N Engl J Med 1988; 318 (24) 1585-1595
    CrossrefPubMedGoogle Scholar
  • 3 Francis CW, Marder VJ. Fibrinolytic therapy for venous thrombosis. Prog Cardiovasc Dis 1991; 34 (03) 193-204
    CrossrefPubMedGoogle Scholar
  • 4 Gersh KC, Nagaswami C, Weisel JW. Fibrin network structure and clot mechanical properties are altered by incorporation of erythrocytes. Thromb Haemost 2009; 102 (06) 1169-1175
    Article in Thieme ConnectPubMedGoogle Scholar
  • 5 Karande GY, Hedgire SS, Sanchez Y. , et al. Advanced imaging in acute and chronic deep vein thrombosis. Cardiovasc Diagn Ther 2016; 6 (06) 493-507
    CrossrefPubMedGoogle Scholar
  • 6 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 (02) 89-98
    Google Scholar
  • 7 Kelly J, Hunt BJ, Moody A. Magnetic resonance direct thrombus imaging: a novel technique for imaging venous thromboemboli. Thromb Haemost 2003; 89 (05) 773-782
    Article in Thieme ConnectPubMedGoogle Scholar
  • 8 Tan M, Mol GC, van Rooden CJ. , et al. Magnetic resonance direct thrombus imaging differentiates acute recurrent ipsilateral deep vein thrombosis from residual thrombosis. Blood 2014; 124 (04) 623-627
    CrossrefPubMedGoogle Scholar
  • 9 Dronkers CEA, Klok FA, van Langevelde K. , et al. Diagnosing recurrent DVT of the leg by two different non-contrast-enhanced magnetic resonance direct thrombus imaging techniques: a pilot study. TH Open 2019; 3 (01) e37-e44
    Article in Thieme ConnectPubMedGoogle Scholar
  • 10 van Dam LF, Dronkers CEA, Gautam G. , et al. Magnetic resonance imaging for diagnosis of recurrent ipsilateral deep vein thrombosis. Blood 2020; 135 (16) 1377-1385
    CrossrefPubMedGoogle Scholar
  • 11 Yamaki T, Nozaki M, Sakurai H. , et al. Combined use of pretest clinical probability score and latex agglutination D-dimer testing for excluding acute deep vein thrombosis. J Vasc Surg 2009; 50 (05) 1099-1105
    CrossrefPubMedGoogle Scholar
  • 12 Rosset A, Spadola L, Ratib O. OsiriX: an open-source software for navigating in multidimensional DICOM images. J Digit Imaging 2004; 17 (03) 205-216
    CrossrefPubMedGoogle Scholar
  • 13 Kuroiwa Y, Yamashita A, Miyati T. , et al. MR signal change in venous thrombus relates organizing process and thrombolytic response in rabbit. Magn Reson Imaging 2011; 29 (07) 975-984
    CrossrefPubMedGoogle Scholar
  • 14 Yamashita A, Matsuda S, Matsumoto T. , et al. Thrombin generation by intimal tissue factor contributes to thrombus formation on macrophage-rich neointima but not normal intima of hyperlipidemic rabbits. Atherosclerosis 2009; 206 (02) 418-426
    CrossrefPubMedGoogle Scholar
  • 15 Yamashita A, Shoji K, Tsuruda T. , et al. Medial and adventitial macrophages are associated with expansive atherosclerotic remodeling in rabbit femoral artery. Histol Histopathol 2008; 23 (02) 127-136
    PubMedGoogle Scholar
  • 16 Nakahashi M, Sato N, Tsushima Y, Amanuma M, Endo K. Diffusion-weighted magnetic resonance imaging of the body in venous thrombosis: a report of four cases. Abdom Imaging 2008; 33 (03) 353-356
    CrossrefPubMedGoogle Scholar
  • 17 Wu G, Morelli J, Xiong Y, Liu X, Li X. Diffusion weighted cardiovascular magnetic resonance imaging for discriminating acute from non-acute deep venous thrombus. J Cardiovasc Magn Reson 2019; 21 (01) 37
    CrossrefPubMedGoogle Scholar
  • 18 Kuroiwa Y, Aburaya M, Yamashita A. , et al. Diffusion-weighted MR imaging of deep vein thrombosis. Magn Reson Med Sci 2016; 15 (01) 144-145
    CrossrefPubMedGoogle Scholar
  • 19 Favrole P, Guichard JP, Crassard I, Bousser MG, Chabriat H. Diffusion-weighted imaging of intravascular clots in cerebral venous thrombosis. Stroke 2004; 35 (01) 99-103
    CrossrefPubMedGoogle Scholar
  • 20 Fineschi V, Turillazzi E, Neri M, Pomara C, Riezzo I. Histological age determination of venous thrombosis: a neglected forensic task in fatal pulmonary thrombo-embolism. Forensic Sci Int 2009; 186 (1-3): 22-28
    CrossrefPubMedGoogle Scholar
  • 21 Ro A, Kageyama N, Tanifuji T, Fukunaga T. Pulmonary thromboembolism: overview and update from medicolegal aspects. Leg Med (Tokyo) 2008; 10 (02) 57-71
    CrossrefPubMedGoogle Scholar
  • 22 Lohr JM, James KV, Deshmukh RM, Hasselfeld KA. Allastair B. Karmody Award. Calf vein thrombi are not a benign finding. Am J Surg 1995; 170 (02) 86-90
    CrossrefPubMedGoogle Scholar
  • 23 Provenzale JM, Engelter ST, Petrella JR, Smith JS, MacFall JR. Use of MR exponential diffusion-weighted images to eradicate T2 “shine-through” effect. AJR Am J Roentgenol 1999; 172 (02) 537-539
    CrossrefPubMedGoogle Scholar
  • 24 Phinikaridou A, Andia ME, Saha P, Modarai B, Smith A, Botnar RM. In vivo magnetization transfer and diffusion-weighted magnetic resonance imaging detects thrombus composition in a mouse model of deep vein thrombosis. Circ Cardiovasc Imaging 2013; 6 (03) 433-440
    CrossrefPubMedGoogle Scholar
  • 25 Ichiki M, Sakai Y, Nango M. , et al. Experimental venous thrombi: MRI characteristics with histopathological correlation. Br J Radiol 2012; 85 (1012): 331-338
    CrossrefPubMedGoogle Scholar
  • 26 Yi J, Thomas LM, Richter-Addo GB. Structure of human R-state aquomethemoglobin at 2.0 Å resolution. Acta Crystallogr Sect F Struct Biol Cryst Commun 2011; 67 (Pt 6): 647-651
    CrossrefPubMedGoogle Scholar
  • 27 Bonekamp S, Corona-Villalobos CP, Kamel IR. Oncologic applications of diffusion-weighted MRI in the body. J Magn Reson Imaging 2012; 35 (02) 257-279
    CrossrefPubMedGoogle Scholar
  • 28 Torkzad MR, Bremme K, Hellgren M. , et al. Magnetic resonance imaging and ultrasonography in diagnosis of pelvic vein thrombosis during pregnancy. Thromb Res 2010; 126 (02) 107-112
    CrossrefPubMedGoogle Scholar
  • 29 Vidmar J, Kralj E, Bajd F, Serša I. Multiparametric MRI in characterizing venous thrombi and pulmonary thromboemboli acquired from patients with pulmonary embolism. J Magn Reson Imaging 2015; 42 (02) 354-361
    CrossrefPubMedGoogle Scholar
  • 30 Hara T, Truelove J, Tawakol A. , et al. 18F-fluorodeoxyglucose positron emission tomography/computed tomography enables the detection of recurrent same-site deep vein thrombosis by illuminating recently formed, neutrophil-rich thrombus. Circulation 2014; 130 (13) 1044-1052
    CrossrefPubMedGoogle Scholar