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Thromb Haemost 2003; 89(05): 773-782
DOI: 10.1055/s-0037-1613461
Review Article
Schattauer GmbH

Magnetic resonance direct thrombus imaging: a novel technique for imaging venous thromboemboli

James Kelly
1   Department. of Haematology, St. Thomas' Hospital, Lambeth, London, UK
,
Beverley J. Hunt
1   Department. of Haematology, St. Thomas' Hospital, Lambeth, London, UK
,
Alan Moody
2   Department of Academic Radiology, QMC, Nottingham, UK
› Author Affiliations
Further Information

Publication History

Received 04 October 2002

Accepted after revision 15 February 2003

Publication Date:
09 December 2017 (online)

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Summary

Invasive testing is now seldom required in patients with suspected venous thromboembolism (VTE). However, a corollary of noninvasive imaging is increased complexity as results are often yielded as probabilities rather than definitive answers and additional testing is frequently required following initial imaging. This creates a milieu in which misunderstandings and protocol violations are common, potentially leading to diagnostic errors. A highly accurate noninvasive imaging technique which allows immediate treatment decisions to be made is needed. Magnetic resonance direct thrombus imaging (MRDTI) is a novel technique which detects methaemoglobin in clot, allowing visualisation of thrombus without using intravenous contrast. It has two major advantages over conventional modalities which identify it as having the potential to fill this role. Firstly, direct visualisation of thrombus overcomes many of the pitfalls of conventional techniques, which have either identified thrombus as a filling defect or in terms of surrogates. Secondly, simultaneous imaging of the legs and chest allows a comprehensive assessment of thrombus load, minimising the importance of overlooked subsegmental pulmonary embolism (PE) and potentially facilitating more titrated treatment.

Early data suggest MRDTI is highly accurate for the detection of both deep vein thrombosis (DVT) and PE, and ongoing outcome studies are evaluating the safety of withholding treatment in suspected DVT and PE on the basis of negative MRDTI alone. If favorable, a multi-centre outcome study evaluating cost-effectiveness as well as safety would be justified. Subject to further evaluation, this technique has the potential greatly to simplify and standardise the investigation of suspected VTE.

Keywords

Magnetic resonance direct thrombus imaging - deep vein thrombosis - pulmonary embolism
 

  • References

  • 1 American Thoracic Society. The diagnostic approach to acute venous thromboembolism: clinical practice guideline.. Am J Respir Crit Care Med 1999; 160: 1043-66.
    CrossrefPubMedGoogle Scholar
  • 2 Pineo GF, Hull RD.. Prevention, diagnosis and management of venous thromboembolic disease. Baillieres Clin Haematol 1998; 11: 541-85.
    CrossrefPubMedGoogle Scholar
  • 3 Wells PS, Hirsh J, Anderson DR, Lensing AW, Foster G, Kearon C, Weitz J, D'Ovidio R, Cogo A, Prandoni P, Girolami A, Ginsberg JS.. A simple clinical model for the diagnosis of deep vein thrombosis combined with impedance plethysmography: potential for an improvement in the diagnostic process. J Intern Med 1998; 243: 15-23.
    CrossrefPubMedGoogle Scholar
  • 4 Wells PS, Anderson DR, Rodger M, Ginsberg JS, Kearon C, Gent M, Turpie AG, Bormanis J, Weitz J, Chamberlain M, Bowie D, Barnes D, Hirsh J.. Derivation of a simple clinical model to categorise patients probability of pulmonary embolism: increasing the model’s utility with the SimpliRED D-dimer. Thromb Haemost 2000; 83: 416-20.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 5 Bernardi E, Prandoni P, Lensing AW, Agnelli G, Guazzaloca G, Scannapieco G, Piovella F, Verlato F, Tomasi C, Moia M, Scarano L, Girolami A.. D-dimer testing as an adjunct to ultrasonography in patients with clinically suspected deep vein thrombosis: prospective cohort study. BMJ 1998; 317: 1037-40.
    CrossrefPubMedGoogle Scholar
  • 6 De Groot MR, van Marwijk, Kooy M, Pouwels JG, Engelage AH, Kuipers BF, Buller HR.. The use of a rapid D-dimer blood test in the diagnostic work up of pulmonary embolism. Thromb Haemost 1999; 82: 1588-92.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 7 Hull R, Hirsh J, Sackett DL, Taylor DW, Carter C, Turpie AG, Powers P, Gent M.. Clinical validity of a negative venogram in patients with clinically suspected venous thrombosis. Circulation 1981; 64: 622-5.
    CrossrefPubMedGoogle Scholar
  • 8 Hull RD, Raskob GE, Coates G, Panju AA.. Clinical validity of a normal perfusion lung scan in patients with suspected pulmonary embolism. Chest 1990; 97: 23-6.
    CrossrefPubMedGoogle Scholar
  • 9 Kipper MS, Moser KM, Kortman KE, Ashburn WL.. Long term follow-up of patients with suspected pulmonary embolism and a normal lung scan. Chest 1982; 82: 411-5.
    CrossrefPubMedGoogle Scholar
  • 10 Kraaijenhagen RA, Piovella F, Bernadi E, Verlato F, Beckers EA, Koopman MM, Barone M, Camporese G, van Loon BJ, Prins MH, Prandoni P, Buller HR.. Simplification of the diagnostic management of suspected deep vein thrombosis. Arch Intern Med 2002; 162: 907-11.
    CrossrefPubMedGoogle Scholar
  • 11 Lensing AW, Hirsh J, Buller HR... Diagnosis of venous thromboembolism. In Colman RW, Hirsh J, Marder VJ, Salzman EW.. eds. Haemostasis and thrombosis: basic principles and clinical practice Philadelphia: JB Lippincott; 1993: 1297-321.
    Google Scholar
  • 12 Stein PD, Athanadoulis C, Alavi A, Greenspan RH, Hales CA, Saltzman HA, Vreim CE, Terrin ML, Weg JG.. Complications and validation of pulmonary angiography in acute pulmonary embolism. Circulation 1992; 85: 462-8.
    CrossrefPubMedGoogle Scholar
  • 13 Perrier A, Desmarais S, Goehring C, de Moerloose P, Morabia A, Unger P, Slosman D, Junod A, Bounameaux H.. D-dimer testing for suspected pulmonary embolism in outpatients. Am J Respir Crit Care Med 1997; 156: 492-6.
    CrossrefPubMedGoogle Scholar
  • 14 Perrier A, Desmarais S, Miron M, de Moerloose P, Lepage R, Slosman D, Didier D, Unger P, Patenaude J, Bounameaux H.. Noninvasive diagnosis of venous thromboembolism in outpatients. Lancet 1999; 353: 190-5.
    CrossrefPubMedGoogle Scholar
  • 15 Van Beek EJ, Kuyer PM, Scheuk B, Brandjes PM, ten Cate JW, Buller HR.. A normal per-fusion lung scan in patients with clinically suspected pulmonary embolism. Chest 1995; 108: 170-3.
    CrossrefPubMedGoogle Scholar
  • 16 Wells PS, Anderson DR, Bormanis J, Guy F, Mitchell M, Gray L, Clement C, Robinson KS, Lewandowski B.. Value of assessment of pretest probability of deep-vein thrombosis in clinical management. Lancet 1997; 350: 1795-8.
    CrossrefPubMedGoogle Scholar
  • 17 Lensing AW, Prandoni P, Prins MH, Buller HR.. Deep vein thrombosis. Lancet 1999; 353: 479-85.
    CrossrefPubMedGoogle Scholar
  • 18 Kearon C, Ginsberg JS, Hirsh J.. The role of venous ultrasonography in the diagnosis of suspected deep vein thrombosis and pulmonary embolism. Ann Intern Med 1998; 129: 1044-9.
    CrossrefPubMedGoogle Scholar
  • 19 The prospective investigation of pulmonary embolism diagnosis (PIOPED) investigators. Value of the ventilation-perfusion scan in acute pulmonary embolism: results of the prospective investigation of pulmonary embolism diagnosis (PIOPED) investigators. J Am Med Assoc 1990; 263: 2753-9.
    CrossrefPubMedGoogle Scholar
  • 20 Berwick DM, Fineberg HV, Weistein MC.. When doctors meet numbers. Am J Med 1981; 71: 991-8.
    CrossrefPubMedGoogle Scholar
  • 21 Birdwell BG, Raskob GE, Whitsett TL, Durica SS, Comp PC, George JN, Tytle TL, McKee PA.. The clinical validity of normal compression ultrasonography in outpatients suspected of having deep venous thrombosis. Ann Intern Med 1998; 128: 1-7.
    CrossrefPubMedGoogle Scholar
  • 22 Cogo A, Lensing AW, Koopman MM, Piovella F, Siragusa S, Wells PS, Villalta S, Buller HR, Turpie AG, Prandoni P.. Compression ultrasonography for diagnostic management of patients with clinically suspected deep vein thrombosis: prospective cohort study. BMJ 1998; 316: 17-20.
    CrossrefPubMedGoogle Scholar
  • 23 Perone P, Bounameaux H, Perrier A.. Comparison of four strategies for diagnosing deep vein thrombosis: cost-effectiveness analysis. Am J Med 2001; 110: 33-40.
    PubMedGoogle Scholar
  • 24 Goldberg SN, Palmer EL, Scott JA, Fisher R... Pulmonary embolism: prediction of the usefulness of initial ventilation perfusion scanning with chest radiographic findings. Radiology 1994; 193: 801-5.
    CrossrefPubMedGoogle Scholar
  • 25 Oudkerk M, van Beek EJ, van Patten WL, Buller HR.. Cost-effectiveness analysis of various strategies in the diagnostic management of pulmonary embolism. Arch Intern Med 1993; 153: 947-54.
    CrossrefPubMedGoogle Scholar
  • 26 Cooper TJ, Hayward WJ, Hartog M.. Survey of the use of pulmonary scintigraphy and angiography for suspected pulmonary thromboembolism in the UK. Clin Radiol 1991; 43: 243-5.
    CrossrefPubMedGoogle Scholar
  • 27 Wells PS, Ginsberg JS, Anderson DR.. et al. Use of a clinical model for safe management of patients with suspected pulmonary embolism. Ann Intern Med 1998; 129: 997-1005.
    CrossrefPubMedGoogle Scholar
  • 28 Dalen JE.. When can treatment be withheld in patients with suspected pulmonary embolism?. Arch Intern Med 1993; 153: 1415-8.
    CrossrefPubMedGoogle Scholar
  • 29 Hull RD, Raskob GE, Ginsberg JS, Panju AA, Brill-Edwards P, Coates G, Pineo GF.. A noninvasive strategy for the treatment of patients with suspected pulmonary embolism. Arch Intern Med 1994; 154: 289-97.
    CrossrefPubMedGoogle Scholar
  • 30 Stein PD, Hull RD, Pineo G.. Strategy that includes serial noninvasive leg tests for diagnosis of thromboembolic disease in patients with suspected acute pulmonary embolism based on data from PIOPED. Arch Intern Med 1995; 155: 2101-4.
    CrossrefPubMedGoogle Scholar
  • 31 Stein PD, Hull RD, Raskob GE.. Withholding treatment in patients with acute pulmonary embolism who have a high risk of bleeding and negative serial non-invasive leg tests. Am J Med 2000; 109: 301-6.
    CrossrefPubMedGoogle Scholar
  • 32 Ferretti GR, Bosson JL, Buffaz PD, Ayanian D, Pison C, Blanc F, Carpentier F, carpentier P, Coulomb M.. Acute pulmonary embolism: role of helical CT scintigraphy in 164 patients with intermediate probability at VQ scintigraphy and normal results at duplex ultrasound of the legs. Radiology 1997; 205: 453-8.
    CrossrefPubMedGoogle Scholar
  • 33 Wells PS, Anderson DR, Rodger M, Stiell I, Dreyer JF, Barnes D, Forgie M, Kovacs G, Ward J, Kovacs MJ.. Excluding pulmonary embolism at the bedside without diagnostic imaging: management of patients with suspected pulmonary embolism presenting to the emergency department by using a simple clinical model and D-dimer. Ann Intern Med 2001; 135: 98-107.
    CrossrefPubMedGoogle Scholar
  • 34 Henschke CI, Mateescul I, Yankelivitz DF.. Changing practice patterns in the workup of pulmonary embolism. Chest 1995; 107: 940-5.
    CrossrefPubMedGoogle Scholar
  • 35 Schluger N, Henschke C, King T, Russo R, Binkert B, Rackson M, hayt D.. Diagnosis of pulmonary embolism at a large teaching hospital. J Thoracic Imaging 1994; 9: 180-4.
    CrossrefPubMedGoogle Scholar
  • 36 Bone RC.. The low probability lung scan – a potentialy lethal reading. Arch Intern Med 1993; 153: 2621-2.
    CrossrefPubMedGoogle Scholar
  • 37 Hull RD, Raskob GE.. Low-probability lung scan findings: a need for change. Ann Intern Med 1991; 114: 142-3.
    CrossrefPubMedGoogle Scholar
  • 38 Cross JJ, Kemp PM, Walsh CG, Flower CD, Dixon AK.. A randomised trial of spiral CT and ventilation perfusion scintigraphy for the diagnosis of pulmonary embolism. Clin Radiol 1998; 53: 177-82.
    CrossrefPubMedGoogle Scholar
  • 39 Kline JA, Johns KH, Colucciello SA, Israel EG.. New diagnostic tests for pulmonary embolism. Ann Emerg Med 2000; 35: 168-80.
    CrossrefPubMedGoogle Scholar
  • 40 Perrier A, Howarth N, Didier D, Loubeyre P, Unger P, de Moerloose P, Slosman D, Junard A, Bounameaux H.. Performance of helical computed tomography in unselected outpatients with suspected Pulmonary embolism. Ann Intern Med 2001; 135: 88-97.
    CrossrefPubMedGoogle Scholar
  • 41 Goodman LR, Lipchik RJ, Kuzo RJ, Liu Y, McAuliffe TL, O’Brien DJ.. Subsequent pulmonary embolism: risk after a negative helical CT pulmonary angiogram – prospective comparison with scintigraphy. Radiology 2000; 215: 535-42.
    CrossrefPubMedGoogle Scholar
  • 42 Musset D, Parent F, Meyer G, Maitre S, Girard P, Leroyer C, Revel M, Carette M, Laurent M, Charbonnier B, Laurent F, Mal H, Nonent M, Lancar R, Grenier P, Simonneau G.. Diagnostic strategy for patients with suspected pulmonary embolism: a prospective multicentre outcome study. Lancet 2002; 360: 1914-20.
    CrossrefPubMedGoogle Scholar
  • 43 Woodward PK.. CT scan negative: where do we go from here?. Radiology 2000; 215: 325-6.
    CrossrefPubMedGoogle Scholar
  • 44 Dixon AK, Coulden RA, Peters AM.. The noninvasive diagnosis of PE. BMJ 2001; 323: 412-3.
    CrossrefPubMedGoogle Scholar
  • 45 Rathbun SW, Raskob GE, Whitsett TL.. Sensitivity and specificity of helical computed tomography in the diagnosis of PE: a systematic review. Ann Intern Med 2000; 132: 227-32.
    CrossrefPubMedGoogle Scholar
  • 46 Cham MD, Yankelevitz DF, Shaham D, Shah AA, Sherman L, Lewis A, Rademaker J, Pearson G, Chri J, Wolff W, Prabhu PM, Galanski M, Clark RA, Sostman HD, Henschke CI.. For the Pulmonary CT Angiography – indirect CT venography Cooperative Group. Deep venous thrombosis: detection by using indirect CT venography. Radiology 2000; 216: 744-51.
    CrossrefPubMedGoogle Scholar
  • 47 Sie P.. The value of laboratory tests in the diagnosis of venous thromboembolism. Haematologica 1995; 80 (Suppl. 02) (suppl.) 57-60.
    PubMedGoogle Scholar
  • 48 Bounameaux H, de Moerloose P.. Plasma measurement of D-dimer as diagnostic aid in suspected venous thromboembolism: an overview. Thromb Haemost 1994; 71: 1– Fraser-6.
    PubMedGoogle Scholar
  • 49 Janes S, Ashford N.. Use of a simplified clinical scoring system and D-dimer testing can reduce the requiremnt for radiology in the exclusion of deep vein thrombosis by over 20%. Br J Haem 2001; 112: 1079-82.
    CrossrefPubMedGoogle Scholar
  • 50 Kruip MJ, Slob MJ, Schijen JH, van der Heul C, Buller HR.. Use of a clinical decision rule in combination with D-dimer concentration in diagnostic work up of patients with suspected pulmonary embolism. Arch Intern Med 2002; 162: 1631-5.
    CrossrefPubMedGoogle Scholar
  • 51 Kearon C, Ginsberg JS, Douketis J, Crowther M, Brill-Edwards P, Weitz JI, Hirsh J.. Management of suspected deep venous thrombosis in outpatients by using clinical assessment and D-dimer testing. Ann Intern Med 2001; 135: 108-11.
    CrossrefPubMedGoogle Scholar
  • 52 Carpenter JP, Holland GA, Baum RA, Owen RS, Carpenter JT, Cope C.. Magnetic resonance venography for the detection of deep vein thrombosis; comparison with contrast venography and duplex Doppler ultrasound. J Vasc Surg 1993; 18: 734-41.
    CrossrefPubMedGoogle Scholar
  • 53 Polak JF, Fox LA.. MR assessment of the extremity veins. Semin Ultrasound CT MR 1999; 20: 36-46.
    CrossrefPubMedGoogle Scholar
  • 54 Montgomery KD, Potter HG, Helfet DL.. Magnetic resonance venography to evaluate the deep venous system of the pelvis in patients who have an acetabular fracture. J Bone Joint Surg 1995; 77: 1639-49.
    CrossrefPubMedGoogle Scholar
  • 55 Spritzer CE, Arata MA, Freed KS.. Isolated pelvic deep venous thrombosis: relative frequency as detected with MR imaging. Radiology 2001; 219: 521-5.
    CrossrefPubMedGoogle Scholar
  • 56 Dupas B, El Kouri D, Curtet C, Peltier P, de Fancal P, Planchou B, Lejeune J.. Angiomagnetic resonance imaging of iliofemorocaval venous thrombosis. Lancet 1995; 346: 17-9.
    CrossrefPubMedGoogle Scholar
  • 57 Erdman WA, Clarke GD.. Magnetic resonance imaging of pulmonary embolism. Semin Ultrasound CT MR 1997; 18: 338-48.
    CrossrefPubMedGoogle Scholar
  • 58 Gefter WB, Hatabu H, Holland GA.. et al. Pulmonary thromboembolism: recent developments in diagnosis with CT and MR imaging. Radiology 1995; 197: 561-74.
    CrossrefPubMedGoogle Scholar
  • 59 Loubeyre P, Revel D, Douek P, Delignette A, Baldy C, Genin G, Amiel M.. Dynamic contrast enhanced MR angiography of pulmonary embolism: comparison with pulmonary angiography. AJR 1993; 162: 1035-9.
    PubMedGoogle Scholar
  • 60 Meaney JF, Weg JG, Chenevert TL, Stafford-Johnson D, Hamilton BH, Prince MR.. Diagnosis of pulmonary embolism with magnetic resonance angiography. New Engl J Med 1997; 336: 1422-7.
    CrossrefPubMedGoogle Scholar
  • 61 Stein PD, Hull RD, Pineo GF.. The role of newer diagnostic techniques in the diagnosis of pulmonary embolism. Curr Opin Pulm Med 1999; 5: 212-5.
    CrossrefPubMedGoogle Scholar
  • 62 Tapson VF.. Pulmonary embolism – new diagnostic approaches. New Engl J Med 1997; 336: 1449-51.
    CrossrefPubMedGoogle Scholar
  • 63 Oudkerk M, van Beek EJ, Wielopolski P, ooijen PM, Brouwers-Kuyper EM, Bongaerts AH, Berghout A.. Comparison of contrast-enhanced magnetic resonance angiography and conventional pulmonary angiography for the diagnosis of pulmonary embolism: a prospective study. Lancet 2002; 359: 1643-7.
    CrossrefPubMedGoogle Scholar
  • 64 Meignan M, Rosso J, Gauthier H, Brunengo F, Claudel S, Sagnard L, d’Azemar P, Simonneau G, Charbonnier B.. Systematic lung scans reveal a high frequency of pulmonary embolism in patients with proximal deep venous thrombosis. Arch Intern Med 2000; 160: 159-64.
    CrossrefPubMedGoogle Scholar
  • 65 Douketis JD, Kearon C, Bates S, Duku EK, Ginsberg JS.. Risk of fatal pulmonary embolism in patients with treated venous thromboembolism. J Am Med Assoc 1998; 279: 458-62.
    CrossrefPubMedGoogle Scholar
  • 66 Grossman RI, Gomori JM, Hackney DB.. et al. Magnetic resonance imaging of haemorrhagic conditions. Acta Radiol. Suppl 1986; 369: 53-5.
    PubMedGoogle Scholar
  • 67 Macchi PJ, Grossman RI, Gomori JM, Goldberg HI, Zimmerman RA, Bilaniuk LT., High field MR.. imaging of cerebral venous thrombosis. Journal of Computer Assisted Tomography 1986; 10: 10-5.
    CrossrefPubMedGoogle Scholar
  • 68 Rapoport S, Sostman HD, Pope C, Camputaro CM, Holcomb W, Gore JC.. Venous clots: evaluation with magnetic resonance imaging. Radiology 1987; 162: 527-30.
    CrossrefPubMedGoogle Scholar
  • 69 Moody AR.. Direct imaging of deep-vein thrombosis with magnetic resonance imaging. Lancet 1997; 350: 1073.
    CrossrefPubMedGoogle Scholar
  • 70 Moody AR, Wastie M, Gregson R, Whitaker SC.. Diagnostic accuracy of direct MR imaging of pulmonary emboli compared to conventional pulmonary angiography. Abstract. Radiology 1997; 205 Suppl 268.
    PubMedGoogle Scholar
  • 71 Moody AR, Liddicoat A, Krapup K.. Pulmonary angiography and direct magnetic resonance imaging of embolus for the detection of pulmonary embolism. Invest Radiol 1997; 32: 431-40.
    CrossrefPubMedGoogle Scholar
  • 72 Moody AR, Pollock JG, O’Connor AR, Bagnall M.. Lower limb deep venous thrombosis: direct MR imaging of the thrombus. Radiology 1998; 209: 349-55.
    CrossrefPubMedGoogle Scholar
  • 73 Fraser DG, Moody AR, Morgan PS, Martel AL, Davidson I.. Diagnosis of lower limb deep venous thrombosis (DVT): a prospective blinded study of magnetic resonance direct thrombus imaging. Ann Intern Med 2002; 136: 89-98.
    CrossrefPubMedGoogle Scholar
  • 74 Bertinin I, Luchinat C... NMR of paramagnetic molecules in biological systems”. Benjamin Cummings, CA; 1986
    Google Scholar
  • 75 Fraser DG, Moody AR, Martel A, Morgan P.. Determinants of D-dimer level in patients presenting with deep venous thrombosis – assessment using magnetic resonance thrombus imaging (Abstract). Haematol J 2000; 1 (Suppl. 01) (Suppl.) 132.
    PubMedGoogle Scholar
  • 76 Fraser DG, Moody AR, Martel A, Morgan p.. Determinants of pulmonary embolism in patients presenting with deep venous thrombosis: prospective study using magnetic resonance direct thrombus imaging (Abstract). Haematol J 2000; 1 (Suppl. 01) (Suppl.) 132-3.
    PubMedGoogle Scholar
  • 77 Fraser DG, Moody AR, Morgan P, Martel A.. Predictors of thrombus age using magnetic resonance direct thrombus imaging (MRDTI) of DVT within the external iliac vein (Abstract). Haematol J 2000; 1 (Suppl. 01) (Suppl.) 133.
    PubMedGoogle Scholar
  • 78 Huisman MV, Beaumont-Koopman MM... The diagnosis of recurrent deep vein thrombosis. In: venous thromboembolism: an evidence-based atlas. Eds. Hull RD, Raskob GE, Pineo GF... New York: Futura Publishing Co; 1996: 147-51.
    Google Scholar
  • 79 Darlington RC, Roughton FJW.. The effect of methaemoglobin on the equilibrium between oxygen and hemoglobin. Am J Physiol 1942; 137: 56-68.
    PubMedGoogle Scholar
  • 80 Cox JST.. The maturation and canalisation of thrombi. Surg Gynec Obstet 1963; 116: 593-9.
    PubMedGoogle Scholar
  • 81 Baldt MM, Zoutsich T, Stumpflu A.. et al. Deep vein thrombosis of the lower extremity: efficacy of spiral CT venography compared to conventional venography in diagnosis. Radiology 1996; 200: 423-8.
    CrossrefPubMedGoogle Scholar
  • 82 Coel MN.. Adequacy of lower limb venous opacification: comparison of supine and upright phlebography. AJR 1980; 134: 163-5.
    CrossrefPubMedGoogle Scholar
  • 83 Rabinov K, Paulin S.. Roentgen diagnosis of venous thrombosis in the leg. Arch Surg 1972; 104: 134-44.
    CrossrefPubMedGoogle Scholar
  • 84 Redman HC.. Deep venous thrombosis: is contrast venography still the diagnostic ‘gold standard’?. Radiology 1988; 168: 277-8.
    CrossrefPubMedGoogle Scholar
  • 85 Gelfland DW, Ott DJ.. Methodologic considerations in comparing imaging methods. AJR 1985; 144: 1117-21.
    CrossrefPubMedGoogle Scholar
  • 86 Clagett PG, Anderson FA, Heit JA, Lieberman JR, Brownell H.. Prevention of venous thromboembolism. Chest 1998; 114(S): 531(S)-60(S).
    CrossrefPubMedGoogle Scholar
  • 87 Girard P, Musset D, Parent F, Maitre S, Phlippoteau C, Simonneau G.. High prevalence of detectable deep venous thrombosis in patients with acute pulmonary embolism. Chest 1999; 116: 903-8.
    CrossrefPubMedGoogle Scholar
  • 88 Havig CO.. Source of pulmonary emboli. Acta Chir Scand 1977; 478 Suppl. 42-7.
    PubMedGoogle Scholar
  • 89 Sandler DA, Martin JF.. Autopsy proven pulmonary embolism in hospital patients: are we detecting enough deep vein thrombosis?. JRSM 1989; 82: 203-5.
    CrossrefPubMedGoogle Scholar
  • 90 Van Beek EJ, Brouwers EM, Song B, Stein PD, Oudkerk M.. Clinical validity of a normal pulmonary angiogram in patients with suspected pulmonary embolism – a critical review. Clin Radiol 2001; 56: 838-42.
    CrossrefPubMedGoogle Scholar
  • 91 Gosselin MV, Rubin GD, Leung AN, Huang J, Rizk NW... Unsuspected pulmonary embolism: prospective detection on routine helical CT scans. Radiology 1998; 208: 209-15.
    CrossrefPubMedGoogle Scholar
  • 92 Crossley I, Moorby S, Macdonald I, Delay S, Moody A.. A randomised trial comparing four methods of investigating patients with suspected pulmonary embolism: the Pulmonary Embolism Diagnosis at Queens (PDQ) Trial. Abstract. Radiology 2001; 221 Suppl 479.
    PubMedGoogle Scholar
  • 93 Crossley I, Moorby S, Macdonald I, Delay S, Moody A.. Magnetic resonance direct clot imaging as a first line test in the evaluation of patients with suspected pulmonary embolism. Abstract. Radiology 2001; 221 Suppl 168.
    PubMedGoogle Scholar
  • 94 Paterson DI, Schwartzman K.. Strategies incorporating spiral CT for the diagnosis of acute pulmonary embolism: A cost-effectiveness analysis. Chest 2001; 119: 1791-800.
    CrossrefPubMedGoogle Scholar
  • 95 Fletcher J, Clark MD, Sutton FA, Wellings R, Garas K.. The cost of MRI: changes in costs from 1989–1996. Br J Radiol 1999; 72: 432-7.
    CrossrefPubMedGoogle Scholar