Journal of Neuro-Oncology

, Volume 101, Issue 3, pp 495–504 | Cite as

Early detection of venous thromboembolism in patients with neuroepithelial tumor: efficacy of screening with serum d-dimer measurements and Doppler ultrasonography

  • Tomohiro Kawaguchi
  • Toshihiro Kumabe
  • Masayuki Kanamori
  • Taigen Nakamura
  • Ryuta Saito
  • Yoji Yamashita
  • Yukihiko Sonoda
  • Mika Watanabe
  • Teiji Tominaga
Clinical Study – Patient Study

Abstract

The efficacy of combined serum d-dimer level measurement and Doppler ultrasonography of the lower extremity was investigated for screening of venous thromboembolism (VTE) in patients with neuroepithelial tumor. Eighty-one patients with neuroepithelial tumor were prospectively studied. All patients underwent measurement of serum d-dimer levels and Doppler ultrasonography of the lower extremity. The serum d-dimer level was measured every week, and Doppler ultrasonography was performed two and two weeks after surgery, then every two weeks until discharge, or every two weeks for patients who did not undergo surgery. If the serum d-dimer level increased over 10.0 μg/ml, Doppler ultrasonography or computed tomography was performed to detect VTE. VTE occurred in 12 (14.8%) patients (seven males and five females; age 34–75, mean 59.0 years). Only one patient was symptomatic, whereas 11 patients identified by the screening were without symptoms. Five patients were treated with anticoagulant therapy, one with prophylactic inferior vena cava filter placement with anticoagulant therapy, and the other six were closely followed up without medication. No patient died of pulmonary embolism. Serial Doppler ultrasonography showed thrombus regression or organization and no thrombus extension. The maximum serum d-dimer value was significantly higher in patients with VTE than in those without VTE (mean 14.5 vs. 3.46 μg/ml, P < 0.001). The d-dimer cutoff value of 5.4 μg/ml could be used to identify VTE with 83% sensitivity and 84% specificity. The combination of sequential serum d-dimer measurement and Doppler ultrasonography of the lower extremity is an efficient and non-invasive procedure for identifying asymptomatic VTE in patients with neuroepithelial tumor.

Keywords

Venous thromboembolism Glioma d-dimer Doppler ultrasonography Pulmonary embolism 

References

  1. 1.
    Heit JA, Silverstein MD, Mohr DN, Petterson TM, O’Fallon WM, Melton LJ III (2000) Risk factors for deep vein thrombosis and pulmonary embolism: a population-based case–control study. Arch Intern Med 160:809–815CrossRefPubMedGoogle Scholar
  2. 2.
    Khorana AA (2003) Malignancy, thrombosis and Trousseau: the case for an eponym. J Thromb Haemost 1:2463–2465CrossRefPubMedGoogle Scholar
  3. 3.
    Khorana AA, Francis CW, Culakova E, Kuderer NM, Lyman GH (2007) Frequency, risk factors, and trends for venous thromboembolism among hospitalized cancer patients. Cancer 110:2339–2346CrossRefPubMedGoogle Scholar
  4. 4.
    Khorana AA, Francis CW, Culakova E, Kuderer NM, Lyman GH (2007) Thromboembolism is a leading cause of death in cancer patients receiving outpatient chemotherapy. J Thromb Haemost 5:632–634CrossRefPubMedGoogle Scholar
  5. 5.
    Chew HK, Wun T, Harvey D, Zhou H, White RH (2006) Incidence of venous thromboembolism and its effect on survival among patients with common cancers. Arch Intern Med 166:458–464CrossRefPubMedGoogle Scholar
  6. 6.
    Sorensen HT, Mellemkjaer L, Olsen JH, Baron JA (1000) Prognosis of cancers associated with venous thromboembolism. N Engl J Med 343:1846–1850CrossRefGoogle Scholar
  7. 7.
    Agnelli G, Piovella F, Buoncristiani P, Severi P, Pini M, D’Angelo A, Beltrametti C, Damiani M, Andrioli GC, Pugliese R, Iorio A, Brambilla G (1998) Enoxaparin plus compression stockings compared with compression stockings alone in the prevention of venous thromboembolism after elective neurosurgery. N Engl J Med 339:80–85CrossRefPubMedGoogle Scholar
  8. 8.
    Semrad TJ, O’Donnell R, Wun T, Chew H, Harvey D, Zhou H, White RH (2007) Epidemiology of venous thromboembolism in 9489 patients with malignant glioma. J Neurosurg 106:601–608CrossRefPubMedGoogle Scholar
  9. 9.
    Stein PD, Beemath A, Meyers FA, Skaf E, Sanchez J, Olson RE (2006) Incidence of venous thromboembolism in patients hospitalized with cancer. Am J Med 119:60–68CrossRefPubMedGoogle Scholar
  10. 10.
    Mack WJ, Ducruet AF, Hickman ZL, Kalyvas JT, Cleveland JR, Mocco J, Schmidt M, Mayer SA, Connolly ES Jr (2008) Doppler ultrasonography screening of poor-grade subarachnoid hemorrhage patients increases the diagnosis of deep venous thrombosis. Neurol Res 9:889–892CrossRefGoogle Scholar
  11. 11.
    Becker DM, Philbrick JT, Abbitt PL (1989) Real-time ultrasonography for the diagnosis of lower extremity deep venous thrombosis. The wave of the future? Arch Intern Med 8:1731–1734CrossRefGoogle Scholar
  12. 12.
    Cogo A, Lensing AW, Wells P, Prandoni P, Buller HR (1995) Noninvasive objective tests for the diagnosis of clinically suspected deep-vein thrombosis. Haemostasis 1–2:27–39Google Scholar
  13. 13.
    Gottlieb RH, Widjaja J, Tian L, Rubens DJ, Voci SL (1999) Calf sonography for detecting deep venous thrombosis in symptomatic patients: experience and review of the literature. J Clin Ultrasound 8:415–420CrossRefGoogle Scholar
  14. 14.
    Kassaï B, Boissel JP, Cucherat M, Sonie S, Shah NR, Leizorovicz A (2004) A systematic review of the accuracy of ultrasound in the diagnosis of deep venous thrombosis in asymptomatic patients. Thromb Haemost 4:655–666Google Scholar
  15. 15.
    Kearon C, Julian JA, Newman TE, Ginsberg JS (1998) Noninvasive diagnosis of deep venous thrombosis. McMaster Diagnostic Imaging Practice Guidelines Initiative. Ann Intern Med 8:663–677Google Scholar
  16. 16.
    Mustafa BO, Rathbun SW, Whitsett TL, Raskob GE (2002) Sensitivity and specificity of ultrasonography in the diagnosis of upper extremity deep vein thrombosis: a systematic review. Arch Intern Med 4:401–404CrossRefGoogle Scholar
  17. 17.
    Segal JB, Eng J, Tamariz LJ, Bass EB (2007) Review of the evidence on diagnosis of deep venous thrombosis and pulmonary embolism. Ann Fam Med 5:63–73CrossRefPubMedGoogle Scholar
  18. 18.
    Wells PS, Lensing AW, Davidson BL, Prins MH, Hirsh J (1995) Accuracy of ultrasound for the diagnosis of deep venous thrombosis in asymptomatic patients after orthopedic surgery. A meta-analysis. Ann Intern Med 1:47–53Google Scholar
  19. 19.
    White RH, McGahan JP, Daschbach MM, Hartling RP (1989) Diagnosis of deep-vein thrombosis using duplex ultrasound. Ann Intern Med 111:297–304PubMedGoogle Scholar
  20. 20.
    Prisco D, Grifoni E (2009) The role of d-dimer testing in patients with suspected venous thromboembolism. Semin Thromb Hemost 35:50–59CrossRefPubMedGoogle Scholar
  21. 21.
    Brown MD, Rowe BH, Reeves MJ, Bermingham JM, Goldhaber SZ (2002) The accuracy of the enzyme-linked immunosorbent assay d-dimer test in the diagnosis of pulmonary embolism: a meta-analysis. Ann Emerg Med 2:133–144CrossRefGoogle Scholar
  22. 22.
    Brown MD, Lau J, Nelson RD, Kline JA (2003) Turbidimetric d-dimer test in the diagnosis of pulmonary embolism: a metaanalysis. Clin Chem 11:1846–1853CrossRefGoogle Scholar
  23. 23.
    Heim SW, Schectman JM, Siadaty MS, Philbrick JT (2004) d-dimer testing for deep venous thrombosis: a metaanalysis. Clin Chem 7:1136–1147CrossRefGoogle Scholar
  24. 24.
    Kobayashi T (2004) [Pulmonary thromboembolism. Deep vein thrombosis (venous thromboembolism)]. Acta Obstet Gynaecol Jpn 56:382–391Google Scholar
  25. 25.
    Stein PD, Hull RD, Patel KC, Olson RE, Ghali WA, Brant R, Biel RK, Bharadia V, Kalra NK (2004) d-dimer for the exclusion of acute venous thrombosis and pulmonary embolism: a systematic review. Ann Intern Med 8:589–602Google Scholar
  26. 26.
    Louis ND (ed) (2007) WHO classification of tumours of the central nervous system. IARC, LyonGoogle Scholar
  27. 27.
    Laporte S, Mismetti P, Décousus H, Uresandi F, Otero R, Lobo JL, Monreal M et al (2008) Clinical predictors for fatal pulmonary embolism in 15,520 patients with venous thromboembolism: findings from the Registro Informatizado de la Enfermedad TromboEmbolica venosa (RIETE) Registry. Circulation 117:1711–1716CrossRefPubMedGoogle Scholar
  28. 28.
    Levitan N, Dowlati A, Remick SC, Tahsildar HI, Sivinski LD, Beyth R, Rimm AA (1999) Rates of initial and recurrent thromboembolic disease among patients with malignancy versus those without malignancy. Risk analysis using Medicare claims data. Medicine 78:285–291CrossRefPubMedGoogle Scholar
  29. 29.
    Kawaguchi T, Kumabe T, Kanamori M, Yamashita Y, Sonoda Y, Watanabe M, Tominaga T (2009) [Venous thromboembolism in patients with malignant glioma]. Jpn J Neurosurg 18:294–299Google Scholar
  30. 30.
    Brandes AA, Scelzi E, Salmistraro G, Ermani M, Carollo C, Berti F, Zampieri P, Baiocchi C, Fiorentino MV (1997) Incidence of risk of thromboembolism during treatment high-grade gliomas: a prospective study. Eur J Cancer 33:1592–1596CrossRefPubMedGoogle Scholar
  31. 31.
    Simanek R, Vormittag R, Hassler M, Roessler K, Schwarz M, Zielinski C, Pabinger I, Marosi C (2007) Venous thromboembolism and survival in patients with high-grade glioma. Neurooncology 9:89–95Google Scholar
  32. 32.
    Ay C, Vormittag R, Dunkler D, Simanek R, Chiriac AL, Drach J, Quehenberger P, Wagner O, Zielinski C, Pabinger I (2009) d-dimer and prothrombin fragment 1 + 2 predict venous thromboembolism in patients with cancer: results from the Vienna Cancer and Thrombosis Study. J Clin Oncol 27:4124–4129CrossRefPubMedGoogle Scholar
  33. 33.
    Eichinger S, Minar E, Bialonczyk C, Hirschl M, Quehenberger P, Schneider B, Weltermann A, Wagner O, Kyrle PA (2003) d-dimer levels and risk of recurrent venous thromboembolism. JAMA 290:1071–1074CrossRefPubMedGoogle Scholar
  34. 34.
    Palareti G, Legnani C, Cosmi B, Guazzaloca G, Pancani C, Coccheri S (2002) Risk of venous thromboembolism recurrence: high negative predictive value of d-dimer performed after oral anticoagulation is stopped. Thromb Haemost 87:7–12PubMedGoogle Scholar
  35. 35.
    Palareti G, Legnani C, Cosmi B, Valdré L, Lunghi B, Bernardi F, Coccheri S (2003) Predictive value of d-dimer test for recurrent venous thromboembolism after anticoagulation withdrawal in subjects with a previous idiopathic event and in carriers of congenital thrombophilia. Circulation 108:313–318CrossRefPubMedGoogle Scholar
  36. 36.
    Kirwan CC, McDowell G, McCollum CN, Kumar S, Byrne GJ (2008) Early changes in the haemostatic and procoagulant systems after chemotherapy for breast cancer. Br J Cancer 99:1000–1006CrossRefPubMedGoogle Scholar
  37. 37.
    Satoh T, Matsumoto K, Uno K, Sakurai M, Okada S, Onuki M, Minaguchi T, Tanaka YO, Homma S, Oki A, Yoshikawa H (2008) Silent venous thromboembolism before treatment in endometrial cancer and the risk factors. Br J Cancer 99:1034–1039CrossRefPubMedGoogle Scholar
  38. 38.
    Ray WZ, Strom RG, Blackburn SL, Ashley WW, Sicard GA, Rich KM (2009) Incidence of deep venous thrombosis after subarachnoid hemorrhage. J Neurosurg 110:1010–1014CrossRefPubMedGoogle Scholar
  39. 39.
    Seidel AC, Cavalheri G Jr, Miranda F Jr (2008) The role of duplex ultrasonography in the diagnosis of lower-extremity deep vein thrombosis in non-hospitalized patients. Int Angiol 5:377–384Google Scholar
  40. 40.
    McQueen AS, Elliott ST, Keir MJ (2009) Ultrasonography for suspected deep vein thrombosis: how useful is single-point augmentation? Clin Radiol 2:148–155CrossRefGoogle Scholar
  41. 41.
    Agnelli G, Radicchia S, Nenci GG (1995) Diagnosis of deep vein thrombosis in asymptomatic high-risk patients. Haemostasis 25:40–48PubMedGoogle Scholar
  42. 42.
    Nurmohamed MT, van Riel AM, Henkens CM, Koopman MM, Que GT, d’Azemar P, Büller HR, ten Cate JW, Hoek JA, van der Meer J, van der Heul C, Turpie AG, Haley S, Sicurella A, Gent M (1996) Low molecular weight heparin and compression stockings in the prevention of venous thromboembolism in neurosurgery. Thromb Haemost 75:233–238PubMedGoogle Scholar
  43. 43.
    Collen JF, Jackson JL, Shorr AF, Moores LK (2008) Prevention of venous thromboembolism in neurosurgery: a metaanalysis. Chest 134:237–249CrossRefPubMedGoogle Scholar
  44. 44.
    Danish SF, Burnett MG, Ong JG, Sonnad SS, Maloney-Wilensky E, Stein SC (2005) Prophylaxis for deep venous thrombosis in craniotomy patients: a decision analysis. Neurosurgery 56:1286–1292CrossRefPubMedGoogle Scholar
  45. 45.
    Seinturier C, Bosson JL, Colonna M, Imbert B, Carpentier PH (2005) Site and clinical outcome of deep vein thrombosis of the lower limbs: an epidemiological study. J Thromb Haemost 3:1362–1367CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC. 2010

Authors and Affiliations

  • Tomohiro Kawaguchi
    • 1
  • Toshihiro Kumabe
    • 1
  • Masayuki Kanamori
    • 1
  • Taigen Nakamura
    • 1
  • Ryuta Saito
    • 1
  • Yoji Yamashita
    • 1
  • Yukihiko Sonoda
    • 1
  • Mika Watanabe
    • 2
  • Teiji Tominaga
    • 1
  1. 1.Department of NeurosurgeryTohoku University Graduate School of MedicineSendaiJapan
  2. 2.Department of PathologyTohoku University HospitalSendaiJapan

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