Imaging Presentation of Venous Thrombosis in Patients With ... - AJR

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Either CT or MRI can be used, particularly when studying central veins. Imaging Presentation of. Venous Thrombosis in Patients. With Cancer. Faisal Khosa1.
N u c l e a r M e d i c i n e a n d M o l e c u l a r I m a g i n g • P i c t o r i a l E s s ay Khosa et al. Venous Thrombosis in Patients With Cancer Nuclear Medicine and Molecular Imaging Pictorial Essay

Imaging Presentation of Venous Thrombosis in Patients With Cancer Faisal Khosa1 Hansel J. Otero 2 Luciano M. Prevedello 3 Frank J. Rybicki 3 Donald N. Di Salvo1,3 Khosa F, Otero HJ, Prevedello LM, Rybicki FJ, Di Salvo DN

OBJECTIVE. The purpose of this article is to review the imaging of venous thrombosis in patients with cancer. CONCLUSION. Multiple imaging techniques have the capacity to display thrombosis accurately. The optimal choice is dictated by the location and duration of symptoms and by the availability of imaging techniques. Peripheral and superficial thrombi are best managed with ultrasound, whereas central thrombi require CT or MRI. If CT and MRI are contraindicated, flow studies are appropriate. FDG PET/CT appropriately shows venous thrombosis and might play a prominent role in the future.

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Keywords: CT, MR, PET, ultrasound, venous thrombosis DOI:10.2214/AJR.09.2501 Received January 30, 2009; accepted after revision September 22, 2009. F. Khosa and H. J. Otero contributed equally to this article. 1 Department of Radiology, Dana Farber Cancer Institute, Boston, MA. 2 Department of Radiology, Tufts Medical Center, 800 Washington St., Boston, MA 02111. Address correspond­ ence to H. J. Otero ([email protected]). 3 Department of Radiology, Brigham and Women’s Hospital, Boston, MA.

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enous thrombosis is a multicausal disorder with a sevenfold increase in incidence and progression in patients with cancer, compared with the general population [1]. Thromboembolic disease occurs with all tumor types [1, 2] and may appear as the first sign of an unsuspected cancer (Fig. 1). The prevalence of occult cancer after an unexplained episode of venous thrombosis is 2.2–12% [3]. The pathogenesis of thrombotic disorders in patients with cancer includes hypercoagulability, venous stasis, and vessel wall damage [2]. Hypercoagulability is a result of indirect pathway activation by production of procoagulants [2]. Venous stasis may be due to reduced mobility (due to cachexia, surgery, or chemotherapy) or to external vascular compression by bulky tumors. Vessel wall damage occurs by direct invasion of vessels, resulting in tumoral thrombosis (Fig. 2), or by indwelling catheters (Fig. 3) that not only cause wall damage but also alter blood flow, increasing the likelihood of venous thrombosis [2, 4]. Clinically, venous thrombosis can be classified as acute, subacute, or chronic. In acute venous thrombosis, thrombi are composed of RBCs, platelets, and fibrin; present with inflammation; and require treatment [5, 6]. In subacute venous thrombosis, the inflammation is subsiding, and the composition of the clot is changing as a result of the loss of heme products [5]. Chronic venous thrombosis can be treated conservatively because

most occluded vein segments are already recanalized, although residual damage is likely [5, 7, 8]. Imaging plays a crucial role in diagnosis or exclusion of venous thrombosis because of the increased risk of venous thrombosis in patients with cancer, the low reliability of clinical signs, and because other clinical markers, such as d-dimer, are not interpretable in patients with cancer [9]. In addition, enhanced spatial resolution, temporal resolution, and tissue characterization of imaging techniques have improved identification of unsuspected venous thrombosis on routine restaging examinations of patients with cancer (~ 6.3% prevalence) [10]. Thus, radiologists need to be aware of the spectrum of venous thrombosis features encountered in the most common imaging techniques used. This article reviews the imaging appearance of venous thrombosis in patients with cancer, as depicted on ultrasound, CT, MRI, radionuclide venography, and combined FDG PET/CT studies. Techniques and Imaging Findings in Venous Thrombosis General Considerations The initial test of choice for diagnosing peripheral venous thrombosis is ultrasound because of its accuracy, low cost, portability, and safety [4, 11]. In addition, Doppler techniques provide direct information regarding flow physiology [12, 13]. Either CT or MRI can be used, particularly when studying central veins.

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Khosa et al. In patients with suspected PE, CT angiography is the standard of care. Nuclear medicine studies include radionuclide imaging, which can be used when CT is contraindicated for PE [14], and PET/CT, which is used for staging and restaging of cancer and which can identify venous thrombosis in those patients [15, 16]. Imaging signs are direct or indirect. Direct signs of venous thrombosis refer to visualization of the thrombus itself (Fig. 4), a filling defect in the vein lumen, abrupt vessel cutoff, or the lack of flow [17, 18]. Indirect signs relate to flow alterations secondary to the thrombus (loss of venous pulsatility or respiratory variation) (Fig. 1), focal organ damage (Fig. 5), global end-organ damage due to back pressure, and hemodynamic changes (i.e., collateral formation or unusual enhancement patterns) [12]. Imaging can also differentiate between acute and chronic thrombi. Acute thrombi are homogeneous, generally expand the lumen, and are located centrally in the vein lumen, possibly with peripheral residual flow. Chronic thrombi are heterogeneous in appearance, have decreased vein diameter, and are peripherally attached to the vein wall [5, 6]. Indirect signs of chronicity include thickened vein walls, central recanalization, reduction in vessel size, presence of collaterals, and end organ atrophy [5, 6, 12]. There is significant variation in the risk of venous thrombosis according to the histologic profile and site of origin of the primary cancer. In general, the highest risk malignancies are uterus, brain, and leukemia [19]. However, certain tumors have a special predilection for involvement of adjacent veins, requiring special attention to those vessels. Remarkable examples include hepatocellular carcinoma, with its tendency to invade the portal veins [20]; renal cell carcinoma and its well-known inclination to invade the renal vein and extend via the inferior vena cava [21]; pancreatic cancer invasion of the splenic-mesenteric-portal complex, leading to extensive perigastric collateral formation [22]; and superior vena cava syndrome caused by extrinsic thoracic venous compression by lung carcinoma and lymphoma [23]. Tumoral thrombus may be distinguished from bland thrombus by identifying one or more of the following characteristics: first, gross direct invasion of tumor parenchyma into the adjacent veins at CT or MRI; second, abnormal arterial vascularity (neovascularity) within the thrombus, in which Doppler ultrasound can show the abnormal low-resistance arterial signals within the thrombus, and in which MRI and CT can show throm-

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bus contrast enhancement; and third, irregular venous lumen expansion. PET/CT does not usually provide additional information regarding bland versus tumoral venous thrombosis differentiation because it can show FDG positivity in both as a result of the presence of inflammatory reaction in each. It should also be noted that cavernous transformation of the portal vein (i.e., the formation of venous channels within or around a previously thrombosed portal vein) might give the appearance of tumoral thrombus by the seeming admixture of arterial and venous signals arising from the recanalized portal vein. The absence of venous expansion or focal parenchymal mass should lead the imager away from the diagnosis of malignancy. Sonographic Findings Real-time and color Doppler sonography are most useful for diagnosis of venous thrombosis in the extremities or neck, where veins are easily accessible, a compressibility test can be performed, and the presence of a clot can be confirmed [24]. Strict attention to technique, with optimization of gray-scale and Doppler flow parameters, is paramount for accurate diagnosis [12]. Color and pulsed Doppler techniques using fast-Fourier transform to display time-velocity data should be used concomitantly so that the absence of detectable color signal is correlated with the absence of visible time velocity tracing; situations where slow flow may be present but difficult to detect (such as portal venous flow in portal hypertension) require the use of maximal gain, low pulse repetition frequency, the absence of wall filters, or the use of power mode. The most sensitive (> 90%) finding of venous thrombosis at ultrasound is the association of a visible thrombus in a vein with an abnormal compressibility test [13] (Fig. 6). In areas of the body not amenable to compression (i.e., subclavian vein or intraabdominal vessels) or regions lacking an adequate sonographic window (i.e., pelvis), reliance on indirect signs is mandatory. In general, on color Doppler, an area of absent flow is indicative of venous thrombosis, and a partial thrombus is outlined by color representing residual flow (Fig. 7). Other indirect signs are lack of response to the Valsalva maneuver, lack of valve motion, and loss of normal pulsatility and respiratory phasicity [12, 25]. In these cases, careful waveform analysis of fast-Fourier transform spectral tracing, rather than the gray-scale or color Doppler image, is of paramount importance.

Acute signs include expansion of the vein lumen and absence of flow. Fresh clots are acoustically only slightly denser than flowing blood and thus appear anechoic. Signs of chronic disease include atretic veins, irregular vessel walls, formation of collateral veins, and increasing clot echogenicity [7, 26] (Fig. 8). CT Findings The first and arguably most important requirement to achieve proper visualization of venous thrombosis at CT is an adequate bolus of contrast for optimal vessel opacification. For routine staging or restaging CT, IV contrast doses of 100 mL are usually used (with the option of reducing it to 75 mL for patients with impaired glomerular filtration rate) with slower injection rates for head and neck (1.0– 1.5 mL/s) and faster rates (2.0 or 2.5 mL/s) for chest, abdomen, or abdomen and pelvis. CT pulmonary angiography for the detection of pulmonary embolism typically uses a higher dose of contrast material (125 mL) at a higher rate (4.0 mL/s), creating a tighter bolus that facilitates the study of the smaller pulmonary branches. It is important to note that newer and faster scanners allow reduction in the total iodine load, an area of active investigation. The mixture of opacified and unopacified blood may mimic venous thrombosis signs, leading to false-positive interpretations of “pseudoclot” [18] (Fig. 9). This is especially likely at the junction of two vessels, one of which has unopacified blood (i.e., at the junction of the brachiocephalic vessels or the azygous junction with the superior vena cava). In these cases, recognition of the characteristic location, careful analysis of blood flow direction, analysis of coronal reformatted images, and close inspection of the suspected “clot” is helpful. A geographic, rather than rounded, “clot”; indistinct “clot” margins; and the posterior layering of denser contrast fluid in a supine patient all argue for a pseudoclot. Problematic cases may require additional studies (Figs. 9B and 9C). Unsuspected deep venous thrombosis and pulmonary embolism are common incidental findings in patients with cancer who undergo routine staging CT studies (6.3% and 3.3%, respectively) [10]. The cardinal sign of acute venous thrombosis and PE at CT is a low-attenuation filling defect that forms an acute angle with the vessel wall or total cutoff of vascular enhancement within the lumen [27, 28] (Figs. 1B and 1C). The filling defect can be complete, partial, or juxtamural. Indirect signs include a high-attenuation rim surrounding the

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Venous Thrombosis in Patients With Cancer filling defect due to contrast material staining in the vasa vasorum, perivenous soft-tissue infiltration representing edema, upstream venous dilation compared with the contralateral side, and prominent collateral veins [27]. Some indirect signs related to altered flow or organ enhancement can be particularly helpful. An example is the enhancement of segment IV of the liver in cases of superior vena cava obstruction, where contrast material follows an abnormal pathway through the internal thoracic vein [29] (Fig. 10). Another disturbance of flow can be appreciated in cases of portal vein thrombosis, in which avid arterial enhancement of the liver parenchyma can be seen in the areas supplied by the thrombosed portal vein (Fig. 11). Reversed or abnormal flow can also be an indirect sign of portal vein thrombosis; cavernous transformation of the portal vein is usually seen in cases of chronic portal vein thrombosis [30]. CT can differentiate between benign and malignant thrombi in hepatocellular carcinoma cases, with 86% sensitivity and 100% specificity [20]. One of the limitations of CT is its inability to differentiate between acute and chronic disease. Some signs of chronicity include recanalization, eccentric flattened defects, and irregular vessel wall [27]. False-positive results may be due to streak artifacts produced by highly concentrated contrast or low-attenuation areas created by parallel vessels running within the axial scanning plane [18]. MR Findings MR techniques are safe, radiation free, and useful for patients with contraindications to contrast-enhanced CT (excluding acute or severe chronic renal failure) [31, 32]. However, the lower spatial resolution, longer examination time, lower availability, and higher cost of MRI make it less practical than CT for venous thrombosis evaluation [28, 33]. Current standard vascular MRI uses 3D gradient-echo sequence and relies on the paramagnetic properties of gadolinium-based contrast agents. The thrombus is identified as a filling defect in the vein lumen. This technique is very useful for imaging the upper extremity veins (Fig. 12) and can also be used in the investigation of central vein thromboses [34, 35] (Fig. 13). The risk of gadolinium-induced toxicity, including nephrogenic systemic fibrosis, has prompted further work with four different unenhanced MR venography flow-independent sequences [36]. First is spin-echo imaging; on these sequences, the flowing blood appears ho-

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mogeneously hypointense (flow void), and the intraluminal thrombus appears as signal residing within the vessel lumen. However, spinecho imaging sequences require long acquisition times and therefore are not widely used. Second is fast spin-echo imaging, which can be used to decrease acquisition times. Using multiple phase-encoded steps per TR, the speed of sequence acquisition is reduced proportionally to the echo-train length. Third, single-shot turbo spin-echo imaging sequences are similar to fast spin-echo imaging sequences and are available from various manufacturers. Fourth, in steady-state free precession imaging, which has relatively high signal-to-noise and contrast-to-noise ratios [37], the thrombus is seen as an intravascular filling defect with low signal intensity, compared with the surrounding hyperintense blood (Fig. 14A). Unenhanced MR venography flow-dependent sequences rely on the flow properties of the blood to provide a signal, using time of flight. Phase-contrast MR venography can also be performed. In time of flight, the thrombus appears as a hypointense filling defect within the hyperintense column of flowing blood (Fig. 14B). However, complex flow patterns (such as flow separation) can generate hemodynamic conditions that are difficult to image with this technique and may contribute to intravascular signal loss [38]. Phase-contrast MR venography detects a phase shift caused by blood flowing through a magnetic field gradient. Spins moving in the direction of increasing gradient strength advance in phase, whereas those moving in the opposite direction fall behind the phase of stationary tissue. The sensitivity of phase-contrast MR venography is highly dependent on the appropriate selection of the velocity-encoding value; this can be particularly challenging in clinical practice and, therefore, this method is rarely used to image the venous system [39]. MRI can also be helpful in differentiating acute versus chronic thrombi [5, 6]. Acute venous thrombosis typically presents as a centrally located filling defect that causes expansion of the affected vein. The thrombus may be partially or completely occlusive and, in the acute setting, is associated with an inflammatory response within the wall of the vein and perivenous tissues. Chronically occluded veins can be poorly visualized because they appear as only a thin fibrotic remnant. At MRI, thrombi gain signal intensity with age on gradient-echo sequences and can, in theory, be differentiated from acute thrombus [5].

Tumor thrombus often enhances as it maintains a vascular supply (Fig. 15), making it possible to differentiate between tumor and bland thrombus. As noted earlier, this differentiation has management implication. Radionuclide Venography Findings Radionuclide studies evaluate the vein lumen by targeting the intravascular blood pool using a radiotracer material. The diseased segment of the vessel shows up as an area of decreased radiotracer activity, because the thrombus reduces or blocks the area containing the radiotracer (Fig. 16). Any asymmetric uptake of the radiotracer, either seen in a vein relative to its contralateral segment or in a contiguous segment of an ipsilateral vein, must be carefully monitored [40]. Other confirmatory signs are delayed tracer transit time, nonuniformity of flow and pooling, venous reflux, and collateral filling [41]. However, a “hot spot” in delayed images can also occur when radiotracer is trapped behind a venous valve [40]. The main limitations of radionuclide venography are that it does not determine the cause of the obstruction or the age of the thrombus and that normal anatomic variants (e.g., duplicate femoral and popliteal veins) can lead to false-positive interpretations [40]. Radionuclide venography is being used less often in light of the increased accuracy of other imaging techniques (i.e., CT and MRI). Nonetheless, it remains valid for evaluating central flow disturbances when CT and MRI are contraindicated. Combined FDG PET/CT Findings Combined FDG PET/CT has emerged as a powerful imaging tool in clinical oncology for the accurate staging and restaging of the majority of cancers. Thus, it is also becoming increasingly important to be able to recognize venous thrombosis during these examinations. FDG PET/CT can show uptake within the vein walls as well as the thrombus itself (Fig. 17). Although some publications have suggested that only tumoral and infected thrombi show increased FDG uptake, a few reports showed that bland thrombus may have this appearance as well, a finding consistent with the acute inflammatory phase of aseptic deep venous thrombosis [15, 16]. In addition, FDG PET may be useful in evaluating response to treatment (i.e., resolution of abnormal FDG PET uptake) [16]. One of the limitations of PET/CT is its inability to distinguish bland from tumoral thrombi. PET is not useful in recognizing the cause of the thrombus, because FDG uptake relies on the degree of re-

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Khosa et al. active inflammation, which is variable and does not correlate with bland or tumor thrombus; because of the intrinsic nature of FDG uptake in the tumor, which itself is variable; and because of the relative amounts of tumor admixed with bland thrombus, which is also quite variable and reduces the chances of correctly identifying the type of thrombus. Summary Multiple imaging techniques have the capacity to display venous thrombosis accurately, and the optimal choice for a particular patient is dictated by a combination of factors, including location and duration of symptoms, availability of different imaging techniques, and local level of expertise for a particular technique. When venous thrombosis is suspected during a routine imaging examination, the first steps are to exclude known technical artifacts and variants that mimic venous thrombosis, such as slow flow states, complex flow patterns, uneven contrast–blood mixing, and normal anatomic variations. In general, peripheral and superficial thrombi are best managed with ultrasound, whereas intracranial, intrathoracic, or abdominopelvic thrombi require a more individualized approach, with CT, MR venography, or nuclear medicine flow studies all being appropriate considerations. At our institution, where both CT and MRI are readily available, the choice is primarily based on issues related to iodinated contrast media administration and patient tolerance for one or the other technique. If CT (i.e., iodinated contrast) and MRI are contraindicated, then nuclear medicine flow studies are appropriate. FDG PET/CT can show both direct and indirect signs of venous thrombosis and can help evaluate response to treatment. It may also play a more prominent role in the evaluation of venous thrombosis in patients with cancer in the near future. References 1. Blom JW, Doggen CJ, Osanto S, Rosendaal FR. Malignancies, prothrombotic mutations, and the risk of venous thrombosis. JAMA 2005; 293:715–722 2. Prandoni P, Piccioli A. Venous thromboembolism and cancer: a two-way clinical association. Front Biosci 1997; 2:e12–e20 3. Monreal M, Trujillo-Santos J. Screening for occult cancer in patients with acute venous thromboembolism. Curr Opin Pulm Med 2007; 13:368–371 4. Polak JF, Yucel EK, Bettmann MA, et al. American College of Radiologists appropriateness criteria: suspected upper extremity deep vein thrombosis. American College of Radiology Website.

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acr.org/SecondaryMainMenuCategories/quality_ safety/app_criteria/pdf/Vascular.aspx. Accessed May 20, 2008 5. Spritzer CE, Trotter P, Sostman HD. Deep venous thrombosis: gradient-recalled-echo MR imaging changes over time—experience in 10 patients. Radiology 1998; 208:631–639 6. Froehlich JB, Prince MR, Greenfield LJ, et al. “Bull’s-eye” sign on gadolinium-enhanced magnetic resonance venography determines thrombus presence and age: a preliminary study. J Vasc Surg 1997; 26:809–816 7. Haenen JH, Wollersheim H, Janssen MC, et al. Evolution of deep venous thrombosis: a 2-year followup using duplex ultrasound scan and strain-gauge plethysmography. J Vasc Surg 2001; 34:649–655 8. Polak JF. Chronic venous thrombosis and venous insufficiency. In: Polak JF. Peripheral vascular sonography: a practical guide, 2nd ed. Philadelphia, PA: Lippincott Williams & Wilkins, 2004:416–417 9. Buller H, Wouter ten Cate J. Primary venous thromboembolism and cancer screening. N Engl J Med 1998; 338:1221–1222 10. Cronin CG, Lohan DG, Keane M, Roche C, Murphy JM. Prevalence and significance of asymptomatic venous thromboembolic disease found on oncologic staging CT. AJR 2007; 189:162–170 11. Polak JF, Yucel EK, Bettmann MA. American College of Radiologists appropriateness criteria: suspected lower extremity deep vein thrombosis. American College of Radiology Website. acr.org/ SecondaryMainMenuCategories/quality_safety/ app_criteria/pdf/Vascular.aspx. Accessed May 20, 2008 12. Blaivas M. Ultrasound in the detection of venous thromboembolism. Crit Care Med 2007; 35[Suppl]: S224–S234 13. Vogel P, Laing FC, Jeffrey RB Jr, Wing VW. Deep venous thrombosis of the lower extremity: US evaluation. Radiology 1987; 163:747–751 14. Bettmann MA, Lyders EM, Yucel EK, et al. American College of Radiologists appropriateness criteria: acute chest pain—suspected pulmonary embolism. American College of Radiology Website. acr.org/SecondaryMainMenuCategories/quality_ safety/app_criteria/pdf/ExpertPanelonCardiovascularImaging.aspx. Accessed May 20, 2008 15. Do B, Mari C, Biswal S, Kalinyak J, Quon A, Gambhir SS. Diagnosis of aseptic deep venous thrombosis of the upper extremity in a cancer patient using fluorine-18 fluorodeoxyglucose positron emission tomography/computerized tomography (FDG PET/CT). Ann Nucl Med 2006; 20:151–155 16. Miceli M, Atoui R, Walker R, et al. Diagnosis of deep septic thrombophlebitis in cancer patients by fluorine-18 fluorodeoxyglucose positron emission tomography scanning: a preliminary report. J

Clin Oncol 2004; 22:1949–1956 17. Woodard PK, Yusen RD. Diagnosis of pulmonary embolism with spiral computed tomography and magnetic resonance angiography. Curr Opin Cardiol 1999; 14:442–447 18. Grenier PA, Beigelman C. Spiral computed tomographic scanning and magnetic resonance angiography for the diagnosis of pulmonary embolism. Thorax 1998; 53:S25–S31 19. Thodiyil PA, Kakkar AK. Variation in relative risk of venous thromboembolism in different cancers. Thromb Haemost 2002; 87:1076–1077 20. Tublin ME, Dodd GD 3rd, Baron RL. Benign and malignant portal vein thrombosis: differentiation by CT characteristics. AJR 1997; 168:719–723 21. Skinner DG, Pritchett TR, Lieskovsky G, et al. Vena caval involvement by renal cell carcinoma: surgical resection provides meaningful long-term survival. Ann Surg 1989; 210:387–392 22. Valls C, Andía E, Sanchez A, et al. Dual-phase helical CT of pancreatic adenocarcinoma: assessment of resectability before surgery. AJR 2002; 178:821–826 23. Wilson LD, Detterbeck FC, Yahalom J. Superior vena cava syndrome with malignant causes. N Engl J Med 2007; 356:1862–1869 24. Chin EE, Zimmerman PT, Grant EG. Sonographic evaluation of upper extremity deep venous thrombosis. J Ultrasound Med 2005; 24:829–838 25. Longley DG, Finlay DE, Letourneau JG. Sonography of the upper extremity and jugular veins. AJR 1993; 160:957–962 26. Murphy TP, Cronan JJ. Evolution of deep venous thrombosis: a prospective evaluation with US. Radiology 1990; 177:543–548 27. Han D, Lee KS, Franquet T, et al. Thrombotic and nonthrombotic pulmonary arterial embolism: spectrum of imaging findings. RadioGraphics 2003; 23:1521–1539 28. Kanne JP, Lalani TA. Role of computed tomography and magnetic resonance imaging for deep venous thrombosis and pulmonary embolism. Circulation 2004; 109:I15–I21 29. Yoshimitsu K, Honda H, Kuroiwa T, et al. Unusual hemodynamics and pseudolesions of the noncirrhotic liver at CT. Radiographics 2001; 21:S81–S96 30. Lee HK, Park SJ, Yi BH, Yeon EK, Kim JH, Hong HS. Portal vein thrombosis: CT features. Abdom Imaging 2008; 33:72–79 31. Clemens S, Leeper KV. Newer modalities for detection of pulmonary emboli. Am J Med 2007; 120:S2–S12 32. Ersoy H, Goldhaber SZ, Cai T, et al. Time-resolved MR angiography: a primary screening examination of patients with suspected pulmonary embolism and contraindications to administration of iodinated contrast material. AJR 2007; 188:1246–1254

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A Fig. 1—78-year-old man with history of right leg swelling for 7 days. A, Ultrasound shows poor respiratory variation in right common femoral vein suspicious for venous thrombosis higher up in pelvic veins. B, CT pulmonary angiography performed in emergency department 3 days later shows multiple bilateral filling defects, including main right pulmonary and inferior segmental arteries (arrows) and heterogeneous well-defined lesion of anterior mediastinum subsequently diagnosed as thymic carcinoma (arrowhead). C, Concurrent CT image shows thrombus expanding right external iliac vein with adjacent fat stranding (arrow).

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Fig. 2—68-year-old man with sarcoma (arrows). A, Anterior aspect of proximal left thigh is shown. B, Lesion invades femoral vein and extends upward to external iliac vein. C and D, Distinction between tumoral thrombus and clot becomes difficult.

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Khosa et al. Fig. 3—32-year-old man with acute myelogenous leukemia. A, Ultrasound image shows peripherally inserted central catheter (arrowheads) in left subclavian vein with absent color Doppler signal. B, Ultrasound image shows absent spectral tracing on pulsed Doppler mode.

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A Fig. 4—Axial CT image showing filling defect with irregular borders inside right atrium (arrow) consistent with thrombus. Note also left hilar and multiple pulmonary metastases from soft-tissue sarcoma (arrowheads).

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Fig. 5—57-year-old man with history of metastatic gastric carcinoma. A, Axial CT image shows filling defect (direct sign) in distal portion of splenic vein (arrow). B, Axial image shows wedge-shaped hypoattenuating areas (straight arrow) consistent with areas of infarct (indirect sign). Curved arrow points to splenic vein.

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Fig. 6—Patient with metastatic retroperitoneal sarcoma. Ultrasound images (B-mode) show positive compressibility test, confirming presence of intraluminal thrombus. A and B, Sagittal (A) and axial (B) images show section where great saphenous vein (GSV) joins common femoral vein (CFV). C, Image shows same area after compression. Both veins are not completely compressible because of presence of intraluminal thrombus. Note higher echogenicity (chronic thrombus) inside GSV (arrowhead) compared with content of CFV (acute thrombus; arrow).

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Venous Thrombosis in Patients With Cancer Fig. 7—57-year-old man with history of pancreatic cancer. Ultrasound images show partial thrombus attached to valve of jugular vein. A, Thrombus is visualized on B-mode as area of higher echogenicity adjacent to valve (arrow). B and C, Thrombus is confirmed on both color Doppler and compressibility test. JV = jugular vein, CCA = common carotid artery.

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Fig. 8—72-year-old woman with multiple myeloma presenting with right upper extremity swelling. A, Ultrasound images show small caliber right jugular vein (arrows) with hyperechogenic material (in comparison with lumen of common carotid artery [CCA]) that does not collapse with compression. B, Color and spectral Doppler images confirmed absence of flow inside chronically thrombosed jugular vein (arrowhead).

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B Fig. 9—64-year-old asymptomatic woman with breast cancer. A, Routine CT restaging examination shows rounded central filling defect (arrow) inside inferior vena cava, suspicious for thrombosis. B, Color and spectral Doppler ultrasound confirmed finding of nonocclusive thrombus in infrahepatic portion of inferior vena cava. C, Notice that in prior CT examination, admixture of opacified and unopacified blood is seen in inferior vena cava at same level. Although this may superficially resemble thrombus, note that difference between two densities is less distinct than in true thrombus.

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Fig. 10—57-year-old woman with history of Hodgkin lymphoma. A, Routine CT examination shows area of avid enhancement predominantly on segment IV of liver, which is suspicious for superior vena cava obstruction. B, Chest CT confirms diagnosis by showing filling defect with irregular borders (arrow) inside superior vena cava consistent with thrombus at level of aortic arch.

Fig. 11—21-year-old man with metastatic malignant peripheral nerve sheath tumor. CT image shows liver hyperenhancement in late arterial phase due to chronic thrombosis of left portal vein. Compensatory enhancement of left lobe by left hepatic artery is seen.

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Venous Thrombosis in Patients With Cancer Fig. 12—24-year-old man with lymphoma and history of long-term left internal jugular and left subclavian central lines. Gadolinium-enhanced MR venography coronal image shows acute left subclavian, internal jugular, and brachiocephalic thrombus (arrows).

Fig. 13—68-year-old woman with uterine cancer complaining of dull abdominal pain. A, Central filling defect (venous thrombus) located inside right ovarian vein (arrow). B, Finding of central filling defect (arrow) was confirmed on gadolinium-enhanced MR venography.

Fig. 14—62-year-old woman with history of pelvic irradiation for cervical cancer. A, Nonocclusive right common iliac thrombus (arrow) is seen with steady-state free precession imaging (Fast Imaging Employing Steady-State Acquisition, GE Healthcare). B, Same thrombus (arrow) is seen on 2D time-of-flight imaging.

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Fig. 15—55-year-old man with left renal cell cancer. A, Left renal cell cancer with tumor (arrowheads) and bland thrombus (arrow) are seen. B, Proximal bland thrombus (arrow) does not show any enhancement after administration of gadolinium contrast, whereas tumoral thrombus shows enhancement (arrowheads). C, Distal tumor (arrowheads) thrombus shows progressive enhancement. Bland thrombus continues to show no enhancement (arrow).

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Fig. 16—Patient with central venous catheter. Radionuclide venography study shows right innominate vein thrombosis. This patient had already undergone upper extremity Doppler examination, with no abnormality seen, and was referred because of strong clinical suspicion. A, No passage of radiotracer is observed in right innominate vein region when injection is performed from right arm, and midline collaterals are seen. B, Normal flow of injected tracer through left arm confirms no disease on this side. C, Radiotracer successfully reaches right cardiac chambers when injection occurs through implantable central venous catheter. Retention of tracer is observed on area of injection.

B Fig. 17—57-year-old man undergoing restaging for colorectal carcinoma. A and B, Maximum-intensity-projection (A) and axial FDG PET (B) images show increased radiotracer uptake (arrow, A) in right pelvis. C and D, Although initially suggestive of pelvic nodal recurrence, expanded right external iliac vein and perivenous inflammatory response (fat stranding) on accompanying CT image (C) and localization of signal to vein on fused image (D) indicate correct diagnosis of acute venous thrombosis. This resolved on followup imaging after patient received anticoagulation therapy.

C

1108

D

AJR:194, April 2010