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Imaging Primary and Secondary Tumor Thrombus of the Inferior Vena Cava: Multi-Detector Computed Tomography and Magnetic Resonance Imaging
Imaging Primary and Secondary Tumor Thrombus of the Inferior Vena Cava: Multi-Detector Computed Tomography and Magnetic Resonance Imaging Carlos Cuevas, MD, Molly Raske, MD, William H. Bush, MD, Thomas Takayama, MD, Jeffrey H. Maki, MD, PhD, Orpheus Kolokythas, MD, and Emily Meshberg, BS
Tumor thrombus of the inferior vena cava (IVC) is a severe medical condition with very poor prognosis unless the patient is treated with surgical resection. It can be caused by a primary leiomyosarcoma originating in the vessel wall or by intraluminal extension of tumor thrombus into the IVC from an adjacent organ. We reviewed 21 cases of tumoral thrombus in the IVC including primary leiomyosarcoma of the IVC (2 cases), renal cell carcinoma (14 cases), adrenocortical carcinoma (2 cases), primary adrenocortical leiomyosarcoma (1 case), hepatocellular carcinoma (1 case), and retroperitoneal metastasis (1 case). The most common findings of IVC tumor thrombus by multi-detector CT and magnetic resonance imaging will be discussed, including scanning protocols and the advantages and disadvantages of each method.
Radiological Assessment of IVC Tumors In view of the poor response of most inferior vena cava (IVC) tumors to chemo- or radiotherapy the only potential curative and/or palliative treatment is surgical resection.1-3 Surgical treatment depends on reliable assessment of tumor extent.1-7 Preoperative radiological study should provide information on identification of the primary tumor, precise delineation of the superior extension of the thrombus in the From the Department of Radiology, University of Washington Medical Center, Seattle, WA. Reprint requests: Carlos Cuevas, MD, University of Washington Medical Center, Department of Radiology, 1959 NE Pacific, Box 357115, HSC BB308, Seattle, WA 98195. E-mail: [email protected]. Curr Probl Diagn Radiol 2006;35:90-101. © 2006 Mosby, Inc. All rights reserved. 0363-0188/2006/$32.00 ⫹ 0 doi:10.1067/j.cpradiol.2006.02.006
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IVC and heart, presence of pulmonary embolism and/or pulmonary metastasis, invasion of the wall of the IVC or spread into other organs, extension into the retroperitoneum, and the presence of Budd– Chiari syndrome. Only two radiological modalities can provide adequate assessment on all these aspects: computed tomography (CT) and magnetic resonance imaging (MRI).4,5,7-9 MRI can acquire images in axial, coronal, or sagittal planes and was thought to be superior to CT because of this ability, although now with the thin-slice protocols of the most advanced MDCT, one has the capability of reformatting the volume of information to display coronal or sagittal images with isotropic voxel resolution (Table 1). Multiphase contrast-enhanced protocols are recommended for an accurate assessment of the tumor thrombus and its complications.5,7 Our MRI protocol includes T2-weighted images as well as multiphase pre- and post-IV contrast injection T1 gradient images. As with other retroperitoneal pathologies, T2- and T1-weighted images are preferred to be acquired with fat saturation. Axial images are better for vessel wall assessment; coronal images provide the best evaluation of proximal tumor extension as well as differentiation between bland and tumor thrombus (Fig 1-9). In preoperative planning it is of utmost importance to detect extension of the tumor into the vessel wall as well as other organs. The capability of diagnosing IVC wall invasion is controversial5,7,10 and in our experience it could be well demonstrated only in some cases (Fig 5).
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TABLE 1. Comparison of MDCT and MR for IVC tumor thrombus imaging
Multiphase capabilities Multiplanar Reformatted Capabilities (MPR)
MDCT
MR
Scanning speed allows for two arterial phases plus multiple other enhanced-phases Isotropic voxel: same resolution in any plane
Not as fast as CT but still can provide multiphasic studies Primary sequence excellent in one plane; MPR from 3D sequences can be of poorer quality depending on resolution Excellent
Accuracy for detecting tumoral thrombus Tissue contrast resolution
Excellent
Spatial resolution Pulmonary embolus diagnosis Radiation dose
Excellent (512 ⫻ 512) Excellent
Good
Better than CT. Can provide good images of the thrombus extension even without the use of IV contrast Generally not as good as CT (256 ⫻ 256) Technically complicated; not as accurate as CT
Elevated for a multiphase angiographic quality study, but medically justified by the severity of the disease and the benefit of an accurate assessment
Proposed Full Multiphase Imaging Protocol 1. Noncontrast: Consider this phase as a baseline when assessing liver or kidney primary masses as well as IVC thrombus to demonstrate enhancement in the subsequent contrast-enhanced series. 2. Early arterial phase (IV contrast bolus timing at both pulmonary and aortic peak enhancement): Consider this for pulmonary embolus detection in the chest. In the abdomen it is useful for detection of arteries recruited by the tumor from adjacent organs (Fig 5). It also demonstrates vessels in the tumor thrombus, allowing differentiation from bland thrombus and is also an effective series for assessing tumor extension into the right atrium of the heart. 3. Late arterial phase (contrast timing: aortic peak ⫹ 15-20 seconds): This phase is good for demonstrating tumoral enhancement and tumor extension into the right atrium of the heart and is mostly useful in the liver if there are hypervascular lesions to assess. 4. Portal venous phase (contrast timing: 60-70 seconds after start of injection): This phase is good for hepatic parenchyma assessment but not useful to assess tumor extension in the IVC because the intraluminal contrast is still too heterogeneous in this phase. Consider using this phase only when hepatic parenchyma assessment is needed. 5. Three-minute delay phase: This phase provides homogeneous enhancement of the IVC lumen and
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No ionizing radiation
therefore allows the best assessment of superior and inferior extension of the tumor. It is useful also for bland (nonenhancing) versus tumor (enhancing) thrombus discrimination. 6. Ten-minute delay phase: This phase is useful for bland versus tumor thrombus discrimination. It shows homogeneous enhancement of the tumor and lumen but no enhancement of the bland thrombus and is particularly useful for Budd– Chiari cases. This phase corresponds to the excretory phase (CT-IVP) and is good for urinary tract assessment, especially in renal tumors or lower IVC tumors that can involve the ureters. 7. Coronal and sagittal reformations can be obtained as required.
Minimal Protocol Proposed 1. Early arterial phase: Chest and abdomen. This phase can be used to rule out pulmonary embolus and lung metastasis and is good for tumoral extent into the right atrium and for feeding vessels in the abdomen. 2. Three-minute-delay phase: Abdomen. This phase can be used for best assessment of the tumoral extent in the IVC and visualization of the primary tumor. The radiation dose can be elevated in multidetector CT (MDCT), especially if the full multiphase protocol is performed. Nevertheless, the
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FIG 1. Primary leiomyosarcoma of the IVC with Budd–Chiari syndrome. Contrast-enhanced CT scan obtained during the arterial phase (A) shows mild heterogeneous enhancement of a tumor thrombus occluding and expanding the IVC; the tumor also spreads into the proximal hepatic veins (arrow). Contrast-enhanced CT scan obtained during the portal-venous phase (B) shows heterogeneous enhancement of the liver parenchyma and lack of enhancement of the hepatic veins. Contrast-enhanced CT scan obtained 3 minutes after injection of contrast (C) provides better images of the tumor thrombus in the IVC; spread of tumor in the expanded proximal hepatic veins (arrow) and nonenhancing thrombus (“bland thrombus”) in the hepatic veins consistent with Budd–Chiari syndrome (arrowhead).
severity of the pathology and the importance of a good presurgical evaluation justify the radiation dose in many of these patients. To keep the radiation dose as low as possible in MDCT, we suggest the use of the minimal protocol if there is only need to evaluate the IVC tumor thrombus extension. If there are other lesions in the abdomen (liver, adrenal, or kidney) that require detection or characterization, the addition of the other phases is suggested.
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Note that a typical portal-venous phase series is not good for IVC thrombus assessment due to the heterogeneous enhancement of the IVC lumen at this phase, making it difficult to discriminate between thrombus and nonopacified blood. This effect is caused by the nonopacified blood coming from the inferior extremities mixing with the highly opacified blood from the renal veins. A 3-minute delay phase provides more homogeneous intralumi-
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FIG 2. Primary leiomyosarcoma of the IVC with intra- and extraluminal growth. Axial T1-weighted MRI (A) demonstrates a hypointense retroperitoneal mass in the region of the IVC. Axial contrast-enhanced T1-weighted MRI obtained during the delayed phase (B) shows homogeneous enhancement of the mass. The IVC has been invaded by the mass and cannot be seen. Axial T2-weighted MRI (C) shows the IVC tumor with heterogeneous high signal. Axial contrast-enhanced CT in portal-venous phase (D) shows similar findings. The appearance of this kind of IVC sarcoma is nonspecific and cannot be differentiated from other retroperitoneal tumors.
nal IVC opacification and therefore is the best phase for thrombus assessment.
Primary Leiomyosarcoma of the IVC Primary leiomyosarcoma of the IVC is a rare malignant tumor originating from the smooth muscle cells of the vessel wall. A review of the world literature demonstrates that the tumor is potentially curable with surgery with 14.2% survival in 10 years.1,11 The mean survival time is about 1 month in inoperable patients and 34 months in those surgically treated.4 According to its location, it can be classified as arising from the
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superior (above the hepatic veins), middle (from the hepatic to the renal veins), and inferior segment (below the renal veins) of the IVC. It is important to accurately describe the location of the tumor because the ones arising in the middle segment have better prognosis than the ones arising from the lower segment: 34.4% versus 0.0% 10-year survival rate.1,11 Metastases have been reported in 40 to 50% of cases.12,13 The tumors can also be classified as predominantly intra- or extraluminal growth. In 73% of the cases the tumor growth is predominantly extraluminal and in 27% is mainly intraluminal.11 In the predominantly intraluminal growth type, the IVC is
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FIG 3. Renal cell carcinoma extending into the IVC: multiplanar reformats and 3D volume rendering of CT images. Sagittal reformat of the arterial phase (A) demonstrates enhancing tumor thrombus in the IVC extending into the right atrium. Coronal reformat in the portal-venous phase (B) showing patency of the right hepatic vein. There are ascites and multiple peritoneal metastases consistent with peritoneal carcinomatosis. 3D volume rendering of the CT images in the arterial phase (C) shows enhancing tumor extending from the right kidney into the heart and through the IVC. The new 64-slice CT with isotropic voxel data acquisition has excellent multiplanar and 3D reformatting capability. (Color version of figure is available online.)
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FIG 4. Renal cell carcinoma IVC thrombus: MRI images. Contrast-enhanced axial T1-weighted MRI (A) shows a large right renal mass continuous with enhancing intraluminal tumor thrombus that expands the right renal vein and extends into the IVC. Normal contralateral renal vein. Coronal T1-weighted post-IV gadolinium (B) provides good assessment of the inferior and superior extension of the tumor. Coronal T2-weighted FR-FSE fat saturated image (C) provides excellent assessment of the tumor extension, comparable with the contrast-enhanced sequences.
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FIG 5. Utility of the angiographic phase (early arterial phase) for tumor thrombus. Contrast-enhanced CT scan (A) and a 3D volume rendering obtained in the early arterial phase (B) demonstrates an artery arising from liver parenchyma and supplying blood to the tumoral thrombus in the IVC (arrows). Recruitment of vessels is typical for large RCC and other hypervascular tumors. The presence of the small hepatic artery feeding the neoplasm proves that the tumor has spread through the IVC wall. In this case no apparent liver invasion could be demonstrated by contrast-enhanced MRI (C and D). (Color version of figure is available online.)
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FIG 6. Adrenocortical carcinoma. Contrast-enhanced axial T1-weighted MRI obtained during venous phase (A) demonstrates a large, heterogeneously enhancing mass in the region of the right adrenal gland. The liver also enhances heterogeneously. The mass invades and expands the intrahepatic portion of the IVC. Delayed phase MRI (B, C) were necessary to show adequate contrast filling of the hepatic veins to exclude tumoral invasion and Budd–Chiari syndrome. Axial T2-weighted MRI at the same level (D) shows heterogeneous signal in the mass and homogeneous signal in the liver.
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level of the diaphragm complicates surgical resection.6 Occasionally, the superior extension of the tumor thrombus is underestimated, such as when a thin cylinder of tumor extends like a “rat tail” from the main thrombus (two patients in our series). In these cases, intraoperative ultrasound was particularly useful to detect this thin component of the thrombus, not seen on CT or MR.
Adrenocortical Carcinoma
FIG 7. Pulmonary tumoral emboli from adrenocortical carcinoma. Axial image from a contrast-enhanced CT scan of the thorax demonstrates thrombus within the left lower lobe pulmonary artery (arrow) in a patient with a large left adrenocortical carcinoma with IVC extension. Thrombus was also present in branches of the right pulmonary artery. Pulmonary endarterectomy was performed and confirmed these to be tumor thrombus.
expanded and leads to IVC obstruction and/or Budd–Chiari syndrome (Fig 1). The diagnosis is easier to suspect in these cases, although differential diagnosis includes hepatocellular carcinoma when the intrahepatic portion of the IVC is involved. In the predominantly extraluminal presentation, the retroperitoneal mass appearance is less specific and the differential diagnosis includes all other retroperitoneal masses such as lymphoma, other sarcomas, metastasis, inflammatory pseudo tumor, and desmoid tumor (Fig 2).
Renal Cell Carcinoma Renal cell carcinoma (RCC) is the most common primary renal tumor in adults.5,14 Spread of the tumor into the IVC occurs in 4 to 10% of the cases.6 In our series, the most common cause for IVC tumor thrombus was RCC (14 of 21). The renal tumor invades and expands the renal vein and the IVC (Figs 3 and 4). Despite extensive involvement of the IVC, patients with no evidence of metastasis have a relative good prognosis with 5-year survival of 32 to 64% after complete surgical resection.5,6,15 It is very important to determine the superior extension of the tumor thrombus since extension beyond the
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Adrenocortical carcinoma is a rare malignancy and can develop at any age; the age distribution is bimodal, with the first peak in the first decade of life, mostly in children ⬍5 years old, and the second peak in the fourth to fifth decade.3,16,17 The tumors are functional or nonfunctional. Functional tumors produce hormones or hormonal precursors resulting in Cushing’s syndrome, virilization syndrome, feminization syndrome, or a combination of Cushing– virilization syndrome.16,17 Typically the entire adrenal gland has been replaced by a heterogeneous mass that displaces the adjacent organs such as the kidney or liver and invades the adrenal vein and IVC (Fig 6). Calcifications are common. Coronal and sagittal images are useful to differentiate right adrenal gland tumors from liver masses. Differential diagnosis includes other adrenal masses like metastasis, pheochromocytoma, or renal cell carcinoma. A large left primary adrenal tumor displacing the kidney and extending into the main left renal vein can mimic an RCC. A rare primary adrenal tumor is the adrenal leiomyosarcoma. Only eight cases have been reported in the English-language literature at the time of this publication.18,19 They usually present as a large mass invading the kidney and adrenal gland with tumor thrombus invading the adrenal veins and IVC indistinguishable from adrenal cell carcinoma (Fig 8). Typically the diagnosis is only made by the pathologist.
Hepatocellular Carcinoma and Other Tumors Hepatocellular carcinoma typically invades the portal veins, although rare advanced cases can invade the hepatic veins and spread into the intrahepatic IVC (Fig 9). Tumoral invasion of the IVC can also
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FIG 8. Large adrenal tumor with IVC extension: adrenal leiomyosarcoma. Contrast-enhanced axial T1-weighted MRIs (A, B) demonstrate a large left adrenal mass with enhancing expansive tumor thrombus in the intrahepatic IVC. Although the thrombus occludes the IVC, Budd–Chiari syndrome is excluded by the presence of normal hepatic vein intraluminal enhancement. Contrast-enhanced T1-weighted MRI obtained during the delayed phase (C) shows the direct extension of tumor from the adrenal gland into the IVC lumen through the left renal vein. Axial T2-weighted MRI (D) shows heterogeneous signal in the tumor.
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FIG 9. Hepatocellular carcinoma invading the IVC. Contrast-enhanced CT with 5-minute delay (A) shows a tumor invading and expanding an accessory right hepatic vein with extension into the IVC (arrow). Enhanced CT at the level of the portal vein (B) shows tumor thrombus in the right portal vein as well as the IVC. In this case the tumoral invasion of the portal vein is key in differentiating this tumor from adrenal cell carcinoma. At a lower level (C) the large exophitic hepatic mass apparently has invaded the right adrenal gland and has displaced the right kidney (not seen). The superior IVC and the hepatic veins are patent in this case (D).
be seen with intrahepatic cholangiocarcinoma and metastasis.20
Conclusion IVC tumor thrombus is a rare and aggressive disease process caused by primary or secondary tumor invasion. Surgical resection is the only known curative treatment. Imaging studies play a central role in diagnosis, staging, and surgical planning. MDCT and MRI are the best methods to evaluate the tumor extension since both have the capability to display images in multiple different planes and can perform multiphasic enhanced studies.
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REFERENCES 1. Mingoli A, Cavallaro A, Sapienza P, et al. International registry of inferior vena cava leiomyosarcoma: Analysis of a world series on 218 patients. Anticancer Res 1996;16: 3201-5. 2. Nessbitt JC, Soltero ER, Dinney CP, et al. Surgical management of renal cell carcinoma with inferior vena cava tumor thrombus. Ann Thorac Surg 1997;63:1592-600. 3. Hedican S, Marshall F. Adrenocortical carcinoma with intracaval extension. J Urol 1997;158:2056-61. 4. Blum U, Wildanger G, Windfuhr M, et al. Preoperative CT and MR imaging of inferior vena cava leiomyosarcoma. Eur J Radiol 1995;20:23-7. 5. Sheth S, Scatarige J, Horton K, et al. Current concepts in the diagnosis and management of renal cell carcinoma: Role of
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6.
7.
8.
9.
10.
11.
multidetector CT and three-dimensional CT. Radiographics 2001;21:S237-54. Staehler G, Brkovic D. The role of radical surgery for renal cell carcinoma: CT, US, MRI, and venacavography. J Urol 2000;163:1671-5. Sohaib A, Teh J, Nargund V, et al. Assessment of tumor invasion of the vena caval wall in renal cell carcinoma cases by magnetic resonance imaging. J Urol 2002;167: 1271-5. Didier D, Racle A, Etievent JP, et al. Tumor thrombus of the inferior vena cava secondary to malignant abdominal neoplasms: US and CT evaluation. Radiology 1987;162: 83-9. Pfluger T, Czekalla R, Hundt C, et al. MR angiography versus color Doppler sonography in the evaluation of renal vessels and the inferior vena cava in abdominal masses of pediatric patients. AJR 1999;173:103-8. Pritchett TR, Raval JK, Benson RC, et al. Peroperative magnetic resonance imaging of vena caval tumor thrombi: Experience with 5 cases. J Urol 1987;138:1220-2. Mingoli A, Feldhaus RJ, Cavallaro A, et al. Leiomyosarcoma of the inferior vena cava: Analysis and search of world literature on 141 patients and report of three new cases. J Vasc Surg 1991;14:688-99.
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12. Griffin AS, Sterchi JM. Primary leimyosarcoma of the inferior vena cava. A case report and review of the literature. J Surg Oncol 1987;34:53-60. 13. Bruyninckx CMA, Derksen OS. Leiomyosarcoma of the inferior vena cava. Case report and review of the literature. J Vasc Surg 1986;3:652-6. 14. American Cancer Society. Cancer facts and figures 2. Atlanta, GA: American Cancer Society, 2000;4. 15. Russo P. Renal cell carcinoma: Presentation, staging, and surgical treatment. Semin Oncol 2000;27:160-76. 16. Ng L, Libertino J. Adrenocortical carcinoma: Diagnosis, evaluation and treatment. J Urol 2003;169:5-11. 17. Wajchenberg B, Albergaria M, Medonca B, et al. Adrenocortical carcinoma, clinical and laboratory observations. Cancer 2000;88:711-36. 18. Kato T, Kato T, Sakamoto S, et al. Primary adrenal leiomyosarcoma with inferior vena cava thrombosis. Int J Clin Oncol 2004;9:189-92. 19. Lujan M, Hoang M. Pleomorphic leiomyosarcoma of the adrenal gland. Arch Pathol Lab Med 2003;127:32-5. 20. Okada Y, Nagino M, Kamiya J, et al. Diagnosis and treatment of inferior vena caval invasion by hepatic cancer. World J Surg 2003;27:689-94.
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Tumor thrombus of the inferior vena cava (IVC) is a severe medical condition with very poor prognosis unless the patient is treated with surgical resection. It can be caused by a primary leiomyosarcoma originating in the vessel wall or by intraluminal extension of tumor thrombus into the IVC from an adjacent organ. We reviewed 21 cases of tumoral thrombus in the IVC including primary leiomyosarcoma of the IVC (2 cases), renal cell carcinoma (14 cases), adrenocortical carcinoma (2 cases), primary adrenocortical leiomyosarcoma (1 case), hepatocellular carcinoma (1 case), and retroperitoneal metastasis (1 case). The most common findings of IVC tumor thrombus by multi-detector CT and magnetic resonance imaging will be discussed, including scanning protocols and the advantages and disadvantages of each method.
Radiological Assessment of IVC Tumors In view of the poor response of most inferior vena cava (IVC) tumors to chemo- or radiotherapy the only potential curative and/or palliative treatment is surgical resection.1-3 Surgical treatment depends on reliable assessment of tumor extent.1-7 Preoperative radiological study should provide information on identification of the primary tumor, precise delineation of the superior extension of the thrombus in the From the Department of Radiology, University of Washington Medical Center, Seattle, WA. Reprint requests: Carlos Cuevas, MD, University of Washington Medical Center, Department of Radiology, 1959 NE Pacific, Box 357115, HSC BB308, Seattle, WA 98195. E-mail: [email protected]. Curr Probl Diagn Radiol 2006;35:90-101. © 2006 Mosby, Inc. All rights reserved. 0363-0188/2006/$32.00 ⫹ 0 doi:10.1067/j.cpradiol.2006.02.006
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IVC and heart, presence of pulmonary embolism and/or pulmonary metastasis, invasion of the wall of the IVC or spread into other organs, extension into the retroperitoneum, and the presence of Budd– Chiari syndrome. Only two radiological modalities can provide adequate assessment on all these aspects: computed tomography (CT) and magnetic resonance imaging (MRI).4,5,7-9 MRI can acquire images in axial, coronal, or sagittal planes and was thought to be superior to CT because of this ability, although now with the thin-slice protocols of the most advanced MDCT, one has the capability of reformatting the volume of information to display coronal or sagittal images with isotropic voxel resolution (Table 1). Multiphase contrast-enhanced protocols are recommended for an accurate assessment of the tumor thrombus and its complications.5,7 Our MRI protocol includes T2-weighted images as well as multiphase pre- and post-IV contrast injection T1 gradient images. As with other retroperitoneal pathologies, T2- and T1-weighted images are preferred to be acquired with fat saturation. Axial images are better for vessel wall assessment; coronal images provide the best evaluation of proximal tumor extension as well as differentiation between bland and tumor thrombus (Fig 1-9). In preoperative planning it is of utmost importance to detect extension of the tumor into the vessel wall as well as other organs. The capability of diagnosing IVC wall invasion is controversial5,7,10 and in our experience it could be well demonstrated only in some cases (Fig 5).
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TABLE 1. Comparison of MDCT and MR for IVC tumor thrombus imaging
Multiphase capabilities Multiplanar Reformatted Capabilities (MPR)
MDCT
MR
Scanning speed allows for two arterial phases plus multiple other enhanced-phases Isotropic voxel: same resolution in any plane
Not as fast as CT but still can provide multiphasic studies Primary sequence excellent in one plane; MPR from 3D sequences can be of poorer quality depending on resolution Excellent
Accuracy for detecting tumoral thrombus Tissue contrast resolution
Excellent
Spatial resolution Pulmonary embolus diagnosis Radiation dose
Excellent (512 ⫻ 512) Excellent
Good
Better than CT. Can provide good images of the thrombus extension even without the use of IV contrast Generally not as good as CT (256 ⫻ 256) Technically complicated; not as accurate as CT
Elevated for a multiphase angiographic quality study, but medically justified by the severity of the disease and the benefit of an accurate assessment
Proposed Full Multiphase Imaging Protocol 1. Noncontrast: Consider this phase as a baseline when assessing liver or kidney primary masses as well as IVC thrombus to demonstrate enhancement in the subsequent contrast-enhanced series. 2. Early arterial phase (IV contrast bolus timing at both pulmonary and aortic peak enhancement): Consider this for pulmonary embolus detection in the chest. In the abdomen it is useful for detection of arteries recruited by the tumor from adjacent organs (Fig 5). It also demonstrates vessels in the tumor thrombus, allowing differentiation from bland thrombus and is also an effective series for assessing tumor extension into the right atrium of the heart. 3. Late arterial phase (contrast timing: aortic peak ⫹ 15-20 seconds): This phase is good for demonstrating tumoral enhancement and tumor extension into the right atrium of the heart and is mostly useful in the liver if there are hypervascular lesions to assess. 4. Portal venous phase (contrast timing: 60-70 seconds after start of injection): This phase is good for hepatic parenchyma assessment but not useful to assess tumor extension in the IVC because the intraluminal contrast is still too heterogeneous in this phase. Consider using this phase only when hepatic parenchyma assessment is needed. 5. Three-minute delay phase: This phase provides homogeneous enhancement of the IVC lumen and
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No ionizing radiation
therefore allows the best assessment of superior and inferior extension of the tumor. It is useful also for bland (nonenhancing) versus tumor (enhancing) thrombus discrimination. 6. Ten-minute delay phase: This phase is useful for bland versus tumor thrombus discrimination. It shows homogeneous enhancement of the tumor and lumen but no enhancement of the bland thrombus and is particularly useful for Budd– Chiari cases. This phase corresponds to the excretory phase (CT-IVP) and is good for urinary tract assessment, especially in renal tumors or lower IVC tumors that can involve the ureters. 7. Coronal and sagittal reformations can be obtained as required.
Minimal Protocol Proposed 1. Early arterial phase: Chest and abdomen. This phase can be used to rule out pulmonary embolus and lung metastasis and is good for tumoral extent into the right atrium and for feeding vessels in the abdomen. 2. Three-minute-delay phase: Abdomen. This phase can be used for best assessment of the tumoral extent in the IVC and visualization of the primary tumor. The radiation dose can be elevated in multidetector CT (MDCT), especially if the full multiphase protocol is performed. Nevertheless, the
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FIG 1. Primary leiomyosarcoma of the IVC with Budd–Chiari syndrome. Contrast-enhanced CT scan obtained during the arterial phase (A) shows mild heterogeneous enhancement of a tumor thrombus occluding and expanding the IVC; the tumor also spreads into the proximal hepatic veins (arrow). Contrast-enhanced CT scan obtained during the portal-venous phase (B) shows heterogeneous enhancement of the liver parenchyma and lack of enhancement of the hepatic veins. Contrast-enhanced CT scan obtained 3 minutes after injection of contrast (C) provides better images of the tumor thrombus in the IVC; spread of tumor in the expanded proximal hepatic veins (arrow) and nonenhancing thrombus (“bland thrombus”) in the hepatic veins consistent with Budd–Chiari syndrome (arrowhead).
severity of the pathology and the importance of a good presurgical evaluation justify the radiation dose in many of these patients. To keep the radiation dose as low as possible in MDCT, we suggest the use of the minimal protocol if there is only need to evaluate the IVC tumor thrombus extension. If there are other lesions in the abdomen (liver, adrenal, or kidney) that require detection or characterization, the addition of the other phases is suggested.
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Note that a typical portal-venous phase series is not good for IVC thrombus assessment due to the heterogeneous enhancement of the IVC lumen at this phase, making it difficult to discriminate between thrombus and nonopacified blood. This effect is caused by the nonopacified blood coming from the inferior extremities mixing with the highly opacified blood from the renal veins. A 3-minute delay phase provides more homogeneous intralumi-
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FIG 2. Primary leiomyosarcoma of the IVC with intra- and extraluminal growth. Axial T1-weighted MRI (A) demonstrates a hypointense retroperitoneal mass in the region of the IVC. Axial contrast-enhanced T1-weighted MRI obtained during the delayed phase (B) shows homogeneous enhancement of the mass. The IVC has been invaded by the mass and cannot be seen. Axial T2-weighted MRI (C) shows the IVC tumor with heterogeneous high signal. Axial contrast-enhanced CT in portal-venous phase (D) shows similar findings. The appearance of this kind of IVC sarcoma is nonspecific and cannot be differentiated from other retroperitoneal tumors.
nal IVC opacification and therefore is the best phase for thrombus assessment.
Primary Leiomyosarcoma of the IVC Primary leiomyosarcoma of the IVC is a rare malignant tumor originating from the smooth muscle cells of the vessel wall. A review of the world literature demonstrates that the tumor is potentially curable with surgery with 14.2% survival in 10 years.1,11 The mean survival time is about 1 month in inoperable patients and 34 months in those surgically treated.4 According to its location, it can be classified as arising from the
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superior (above the hepatic veins), middle (from the hepatic to the renal veins), and inferior segment (below the renal veins) of the IVC. It is important to accurately describe the location of the tumor because the ones arising in the middle segment have better prognosis than the ones arising from the lower segment: 34.4% versus 0.0% 10-year survival rate.1,11 Metastases have been reported in 40 to 50% of cases.12,13 The tumors can also be classified as predominantly intra- or extraluminal growth. In 73% of the cases the tumor growth is predominantly extraluminal and in 27% is mainly intraluminal.11 In the predominantly intraluminal growth type, the IVC is
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FIG 3. Renal cell carcinoma extending into the IVC: multiplanar reformats and 3D volume rendering of CT images. Sagittal reformat of the arterial phase (A) demonstrates enhancing tumor thrombus in the IVC extending into the right atrium. Coronal reformat in the portal-venous phase (B) showing patency of the right hepatic vein. There are ascites and multiple peritoneal metastases consistent with peritoneal carcinomatosis. 3D volume rendering of the CT images in the arterial phase (C) shows enhancing tumor extending from the right kidney into the heart and through the IVC. The new 64-slice CT with isotropic voxel data acquisition has excellent multiplanar and 3D reformatting capability. (Color version of figure is available online.)
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FIG 4. Renal cell carcinoma IVC thrombus: MRI images. Contrast-enhanced axial T1-weighted MRI (A) shows a large right renal mass continuous with enhancing intraluminal tumor thrombus that expands the right renal vein and extends into the IVC. Normal contralateral renal vein. Coronal T1-weighted post-IV gadolinium (B) provides good assessment of the inferior and superior extension of the tumor. Coronal T2-weighted FR-FSE fat saturated image (C) provides excellent assessment of the tumor extension, comparable with the contrast-enhanced sequences.
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FIG 5. Utility of the angiographic phase (early arterial phase) for tumor thrombus. Contrast-enhanced CT scan (A) and a 3D volume rendering obtained in the early arterial phase (B) demonstrates an artery arising from liver parenchyma and supplying blood to the tumoral thrombus in the IVC (arrows). Recruitment of vessels is typical for large RCC and other hypervascular tumors. The presence of the small hepatic artery feeding the neoplasm proves that the tumor has spread through the IVC wall. In this case no apparent liver invasion could be demonstrated by contrast-enhanced MRI (C and D). (Color version of figure is available online.)
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FIG 6. Adrenocortical carcinoma. Contrast-enhanced axial T1-weighted MRI obtained during venous phase (A) demonstrates a large, heterogeneously enhancing mass in the region of the right adrenal gland. The liver also enhances heterogeneously. The mass invades and expands the intrahepatic portion of the IVC. Delayed phase MRI (B, C) were necessary to show adequate contrast filling of the hepatic veins to exclude tumoral invasion and Budd–Chiari syndrome. Axial T2-weighted MRI at the same level (D) shows heterogeneous signal in the mass and homogeneous signal in the liver.
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level of the diaphragm complicates surgical resection.6 Occasionally, the superior extension of the tumor thrombus is underestimated, such as when a thin cylinder of tumor extends like a “rat tail” from the main thrombus (two patients in our series). In these cases, intraoperative ultrasound was particularly useful to detect this thin component of the thrombus, not seen on CT or MR.
Adrenocortical Carcinoma
FIG 7. Pulmonary tumoral emboli from adrenocortical carcinoma. Axial image from a contrast-enhanced CT scan of the thorax demonstrates thrombus within the left lower lobe pulmonary artery (arrow) in a patient with a large left adrenocortical carcinoma with IVC extension. Thrombus was also present in branches of the right pulmonary artery. Pulmonary endarterectomy was performed and confirmed these to be tumor thrombus.
expanded and leads to IVC obstruction and/or Budd–Chiari syndrome (Fig 1). The diagnosis is easier to suspect in these cases, although differential diagnosis includes hepatocellular carcinoma when the intrahepatic portion of the IVC is involved. In the predominantly extraluminal presentation, the retroperitoneal mass appearance is less specific and the differential diagnosis includes all other retroperitoneal masses such as lymphoma, other sarcomas, metastasis, inflammatory pseudo tumor, and desmoid tumor (Fig 2).
Renal Cell Carcinoma Renal cell carcinoma (RCC) is the most common primary renal tumor in adults.5,14 Spread of the tumor into the IVC occurs in 4 to 10% of the cases.6 In our series, the most common cause for IVC tumor thrombus was RCC (14 of 21). The renal tumor invades and expands the renal vein and the IVC (Figs 3 and 4). Despite extensive involvement of the IVC, patients with no evidence of metastasis have a relative good prognosis with 5-year survival of 32 to 64% after complete surgical resection.5,6,15 It is very important to determine the superior extension of the tumor thrombus since extension beyond the
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Adrenocortical carcinoma is a rare malignancy and can develop at any age; the age distribution is bimodal, with the first peak in the first decade of life, mostly in children ⬍5 years old, and the second peak in the fourth to fifth decade.3,16,17 The tumors are functional or nonfunctional. Functional tumors produce hormones or hormonal precursors resulting in Cushing’s syndrome, virilization syndrome, feminization syndrome, or a combination of Cushing– virilization syndrome.16,17 Typically the entire adrenal gland has been replaced by a heterogeneous mass that displaces the adjacent organs such as the kidney or liver and invades the adrenal vein and IVC (Fig 6). Calcifications are common. Coronal and sagittal images are useful to differentiate right adrenal gland tumors from liver masses. Differential diagnosis includes other adrenal masses like metastasis, pheochromocytoma, or renal cell carcinoma. A large left primary adrenal tumor displacing the kidney and extending into the main left renal vein can mimic an RCC. A rare primary adrenal tumor is the adrenal leiomyosarcoma. Only eight cases have been reported in the English-language literature at the time of this publication.18,19 They usually present as a large mass invading the kidney and adrenal gland with tumor thrombus invading the adrenal veins and IVC indistinguishable from adrenal cell carcinoma (Fig 8). Typically the diagnosis is only made by the pathologist.
Hepatocellular Carcinoma and Other Tumors Hepatocellular carcinoma typically invades the portal veins, although rare advanced cases can invade the hepatic veins and spread into the intrahepatic IVC (Fig 9). Tumoral invasion of the IVC can also
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FIG 8. Large adrenal tumor with IVC extension: adrenal leiomyosarcoma. Contrast-enhanced axial T1-weighted MRIs (A, B) demonstrate a large left adrenal mass with enhancing expansive tumor thrombus in the intrahepatic IVC. Although the thrombus occludes the IVC, Budd–Chiari syndrome is excluded by the presence of normal hepatic vein intraluminal enhancement. Contrast-enhanced T1-weighted MRI obtained during the delayed phase (C) shows the direct extension of tumor from the adrenal gland into the IVC lumen through the left renal vein. Axial T2-weighted MRI (D) shows heterogeneous signal in the tumor.
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FIG 9. Hepatocellular carcinoma invading the IVC. Contrast-enhanced CT with 5-minute delay (A) shows a tumor invading and expanding an accessory right hepatic vein with extension into the IVC (arrow). Enhanced CT at the level of the portal vein (B) shows tumor thrombus in the right portal vein as well as the IVC. In this case the tumoral invasion of the portal vein is key in differentiating this tumor from adrenal cell carcinoma. At a lower level (C) the large exophitic hepatic mass apparently has invaded the right adrenal gland and has displaced the right kidney (not seen). The superior IVC and the hepatic veins are patent in this case (D).
be seen with intrahepatic cholangiocarcinoma and metastasis.20
Conclusion IVC tumor thrombus is a rare and aggressive disease process caused by primary or secondary tumor invasion. Surgical resection is the only known curative treatment. Imaging studies play a central role in diagnosis, staging, and surgical planning. MDCT and MRI are the best methods to evaluate the tumor extension since both have the capability to display images in multiple different planes and can perform multiphasic enhanced studies.
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