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Tumoral Pulmonary Emboli From Angioinvasive Hepatocellular Carcinoma
Tumoral Pulmonary Emboli From Angioinvasive Hepatocellular Carcinoma Toshimasa Clark, MD,a Suresh Maximin, MD,a Jabi Shriki, MD,b and Puneet Bhargava, MDb
Tumoral pulmonary emboli from hepatocellular carcinoma (HCC) have rarely been described, although invasion of the portal and hepatic venous systems is a well-known complication. HCC originating in a noncirrhotic liver in the absence of chronic hepatitis B infection is also uncommon. We present a case of a patient with chronic hepatitis C infection without hepatic cirrhosis who developed angioinvasive HCC with intracardiac extension and tumoral pulmonary emboli. Differential considerations, including combined HCC-cholangiocarcinoma, other hepatic mesenchymal tumors, and metastasis, are discussed. Owing to poor prognosis, no resection was attempted. Autopsy was performed because of the unusual clinical presentation, and immunohistochemistry of the hepatic tumor, the intracardiac extension, and the pulmonary emboli were concordant with hepatocellular origin. Even though definitive diagnosis may not affect patient outcome, it is important for radiologists and clinicians to be aware that angioinvasive HCC may arise in the absence of cirrhosis.
Introduction Hepatocellular carcinoma (HCC) includes most primary liver cancers. Rates of mortality and ageadjusted incidence have been documented in large series to be rising since 1976. There is higher incidence and mortality of HCC in men than in women and in black individuals as compared with white individuals. There is also increased incidence with age, with peak incidence among white men at approximately the age of 75 years.1 Prognostic factors From the aDepartment of Radiology, University of Washington, Seattle, WA; and bVA Puget Sound Health Care System, Seattle, WA. Reprint requests: Toshimasa Clark, MD, Department of Radiology, University of Washington, 1959 NE Pacific St, Box 357115, Seattle, WA 98195. E-mail: [email protected]. Curr Probl Diagn Radiol 2014;43:227–231. Published by Mosby, Inc. 0363-0188/$36.00 + 0 http://dx.doi.org/10.1067/j.cpradiol.2014.04.006
Curr Probl Diagn Radiol, July/August 2014
include age, presence of cirrhosis, tumor size, and adjuvant chemotherapy if resected.2 Imaging features characteristic for conventional HCC are as defined on the American College of Radiology's Liver Imaging and Reporting System, namely late arterial phase hyperenhancement, delayed phase hypoenhancement relative to liver parenchyma, and a delayed phase enhancing peripheral pseudocapsule.3 There exist well-defined, algorithmic imaging criteria such that categorization of observations into strata ranked by their probability of representing HCC is possible in a semiautomated fashion.4 Invasion of the portal and hepatic venous systems is a well-described finding seen in HCC, although extension into the inferior vena cava and right atrium is rare.5,6 The longest reported survival time for a patient with HCC with cardiac extension is 26 months.7 The surgical technique for resection of tumor with cardiac extension involves cardiopulmonary bypass, which may represent an unacceptable risk given the data indicating little potentially low long-term benefit. Treatment options for HCC include resection when surgically feasible, transplant, systemic chemotherapy, and locoregional therapies, including radiofrequency ablation, cryoablation, Yttrium-90 chemoembolization, and irreversible electroporation.8-11 Here, the authors present a case of HCC arising in a patient without hepatic cirrhosis, with the rare disease manifestations of both proven intracardiac extension and tumoral pulmonary emboli. In addition to the unusual clinical presentation, the imaging findings were atypical for HCC. Differential considerations included combined HCC-cholangiocarcinoma (HCC-CC), other hepatic mesenchymal tumors, and metastasis.
Methods This study was approved by our institutional review board. Computed tomography (CT) images with
227
FIG 1. Axial contrast-enhanced CT demonstrates a 7-cm mass in the Couinaud segment 7 that is hypervascular during the late arterial phase (left panel; arrow) and isodense without washout on delayed imaging (right panel; arrowhead).
intravenous contrast were acquired in late arterial, portal venous, and 5-minute delayed phases on an HD 750 64-slice scanner (GE Healthcare; Little Chalfont, Buckinghamshire, United Kingdom). Gross pathologic photography was performed with a 5D Mark II camera body and 24-105 mm f/4L IS lens (Canon, Inc; Tokyo, Japan), with postprocessing performed in Lightroom (Adobe, Inc; San Jose, CA). The clinical notes, laboratory data, and autopsy report were accessed through our institution's electronic medical record.
Case Report Our patient was a 65-year-old man with a history of chronic hepatitis C without hepatic cirrhosis who presented with 1 week of increased dyspnea on exertion, periumbilical abdominal pain, and malaise, following 6 months of similar, progressive symptoms. Right upper quadrant US demonstrated a thrombus within the inferior vena cava. A multiphase liverprotocol contrast-enhanced abdominal CT was subsequently performed. CT scan of the liver demonstrated a noncirrhotic liver morphology. There was a 7-cm infiltrative, arterially enhancing mass in the Couinaud hepatic segment 7 that became isodense on delayed phase imaging (Fig 1), without unequivocal washout relative to adjacent hepatic parenchyma. Enhancing thrombus was present with both a striated appearance and “thread-and-streak sign,” with extension into the hepatic veins, inferior vena cava,
228
and right atrium (Fig 2). The right atrium was nearly occluded by this thrombus. Owing to the extensive vascular invasion and near occlusion of the right atrium by presumed tumor thrombus, multidisciplinary assessment was that chemotherapeutic or surgical intervention would not prolong survival or palliate the patient's condition. The patient was placed on comfort care measures and died on the fourth hospital day with respiratory failure and asystole secondary to lactic acidosis. Test for alphafetoprotein level was incomplete, pending processing by the laboratory before the patient's death, and further laboratory assessment was halted at that point. Autopsy was performed, confirming the infiltrative hepatic mass as angioinvasive HCC arising in a noncirrhotic liver (Fig 3). There was tumoral
FIG 2. Coronal reformatted image from late arterial phase contrastenhanced CT demonstrates tumoral thrombus from HCC extending into the hepatic veins, inferior vena cava, and right atrium (arrow).
Curr Probl Diagn Radiol, July/August 2014
FIG 3. Sectioned liver from autopsy demonstrates primary HCC within right hepatic lobe (arrow) as well as HCC tumor thrombus within hepatic veins (arrowhead). Note the pathologic “thread-andstreak sign” and striated appearance of the tumor thrombus. (Color version of figure is available online.)
extension of HCC into the hepatic veins, inferior vena cava, and right atrium (Figs 3 and 4). The lungs were sectioned to assess the cause of the patient's respiratory failure. The large right atrial tumor thrombus and multiple pulmonary emboli were confirmed to be of HCC origin (Figs 4 and 5).
Discussion The main differential diagnoses considered in this case included HCC, combined HCC-CC, other primary hepatic mesenchymal tumors, and hypervascular metastases.8,12-15 In this case, HCC was suspected, although the patient did not have hepatic cirrhosis. Definitive diagnosis of HCC was confirmed at autopsy.
FIG 4. Heart seen at autopsy demonstrates a large HCC tumor thrombus adherent to the wall of the right atrium (arrow). (Color version of figure is available online.)
Curr Probl Diagn Radiol, July/August 2014
FIG 5. Sectioned lung at autopsy demonstrates HCC tumoral emboli within multiple pulmonary arteries (arrows). (Color version of figure is available online.)
When HCC arises in patients without cirrhosis, data from small series suggest that it does so at a younger age, is more common in women, and is less likely to be associated with elevated alpha-fetoprotein.16 These demographic characteristics may be region dependent, as another series of patients seen at the University of Pittsburgh who developed HCC in the absence of hepatic cirrhosis demonstrated a male predominance and wide age range.17 The incidence of HCC arising in cirrhotic vs noncirrhotic livers also demonstrates geographical variation, with Tiribelli et al reporting that 87% of cases of HCC in Trieste, Italy, and 81% of cases of HCC in Chiba, Japan, arose in patients with underlying hepatic cirrhosis.18 Fibrolamellar HCC typically arises in younger patients without hepatic cirrhosis. Characteristic imaging features include arterial hyperenhancement and a hypodense, T2hypointense central scar, often with calcification.19 In this case, imaging findings and patient demographics were inconsistent with fibrolamellar HCC, although hepatic cirrhosis was absent. HCC-CC has been reported to have imaging features that overlap with those of HCC and cholangiocarcinoma, which may reflect origin from a common progenitor cell. Reported sensitivity and accuracy of imaging is low, with Fowler et al13 reporting sensitivities and specificities of 33%-34% and 81%-100% for 2 readers. In this case, although the imaging features of the primary hepatic lesion and tumoral thrombus were not classic for HCC, they were not typical for cholangiocarcinoma either, with a lack of progressive delayed enhancement. Metastases to the liver are typically hypovascular. As per a large series conducted by Danet et al,14
229
hypervascular metastases typically show peripheral enhancement in the arterial phase, with adjacent hypoenhancement and central progressive enhancement during the delayed phase. Primary malignancies associated with a higher incidence of hypervascular metastases include breast carcinoma, carcinoid, neuroendocrine tumor, renal cell carcinoma, and thyroid carcinoma.14,15 Other tumors may arise from the mesenchymal cells of the liver and demonstrate a diverse set of imaging features. Angiosarcoma is the primary differential consideration among these given imaging findings of arterial phase hyperenhancement. The classic history of distant prior exposure to Thorotrast contrast is now seen in a minority of patients found to have hepatic angiosarcoma, and its imaging appearance varies from a solid mass with progressive enhancement to a predominantly cystic lesion with only peripheral enhancement.12,20,21 The appearance of the hepatic angioinvasive mass in this case was not incompatible with angiosarcoma, but there were no imaging features suggesting this diagnosis specifically. This case represents an instance of angioinvasive HCC arising in a noncirrhotic liver, the incidence of demonstrates geographical variability. Documentation of pathology-proven tumoral emboli to the pulmonary arteries from HCC is exceptionally rare, with prior reports of tumoral emboli arising from sarcomas, germ cell tumors, and carcinomas of the prostate, breast, stomach, pancreas, and liver.22-27 It is important for radiologists and clinicians to be aware that angioinvasive HCC may arise in the absence of cirrhosis, even though definitive diagnosis may not affect patient outcome if the patient presents at an advanced stage of disease, such as in the case of our patient.
REFERENCES 1. El-Serag HB, Mason AC. Rising incidence of hepatocellular carcinoma in the United States. N Engl J Med 1999;340 (10):745-50. 2. Nagasue N, Kohno H, Chang Y, et al. Liver resection for hepatocellular carcinoma: results of 229 consecutive patients during 11 years. Ann Surg 1993;217(4):375-84. 3. Radiology ACo. Liver imaging reporting and data system version 2013.1, 2013. 4. Clark TJ, McNeeley MF, Maki JH. Design and implementation of handheld and desktop software for the structured reporting of hepatic masses using the LI-RADS schema. Acad Radiol 2014;21(4):491-506. 5. McBride K, Masterson J. The thread and streak sign of portal vein tumour thrombus demonstrated by colour Doppler imaging. Br J Radiol 1992;65(775):607-9.
230
6. Raab BW. The thread and streak sign. Radiology 2005;236 (1):284-5. 7. Wu CC, Hseih S, Ho W, et al. Surgical treatment for recurrent hepatocellular carcinoma with tumor thrombi in right atrium: Using cardiopulmonary bypass and deep hypothermic circulatory arrest. J Surg Oncol 2000;74:227-31. 8. Ryder SD. Guidelines for the diagnosis and treatment of hepatocellular carcinoma (HCC) in adults. Gut 2003; 52(suppl III):iii1-8. 9. Lu DS, Yu NC, Raman SS, et al. Radiofrequency ablation of hepatocellular carcinoma: Treatment success as defined by histologic examination of the explanted liver. Radiology 2005;234:954-60. 10. Bhargava P, Vaidya S, Dick AA, et al. Imaging of orthotopic liver transplantation: Review. Am J Roentgenol 2011;196 (suppl 3):WS15-25 [Quiz S35-8]. 11. Shin DS, Dighe MK, Wang C, et al. Surgical resection of a malignant liver lesion: What the surgeon wants the radiologist to know. Am J Roentgenol, in press. 12. Bhargava P, Iyer RS, Moshiri M, et al. Radiologic-pathologic correlation of uncommon mesenchymal liver tumors. Curr Prob Diagn Radiol 2013;42(5):183-90. 13. Fowler KJ, Sheybani A, Parker RA 3rd, et al. Combined hepatocellular and cholangiocarcinoma (biphenotypic) tumors: Imaging features and diagnostic accuracy of contrast-enhanced CT and MRI. Am J Roentgenol 2013;201(2):332-9. 14. Danet IM, Semelka RC, Leonardou P, et al. Spectrum of MRI appearances of untreated metastases of the liver. Am J Roentgenol 2003;181:809-17. 15. Sica GT, Hoon Ji, Ros PR. CT and MR imaging of hepatic metastases. Am J Roentgenol 2000;174:691-8. 16. Melia WM, Wilkinson ML, Portmann BC, et al. Hepatocellular carcinoma in the non-cirrhotic liver: A comparison with that complicating cirrhosis. Q J Med 1984;53(211):391-400. 17. Brancatelli G, Federle MP, Grazioli L, et al. Hepatocellular carcinoma in noncirrhotic liver: CT, clinical, and pathologic findings in 39 U.S. residents. Radiology 2002;222(1):89-94. 18. Tiribelli C, Melato M, Croce LS, et al. Prevalence of hepatocellular carcinoma and relation to cirrhosis: Comparison of two different cities of the world—Trieste, Italy, and Chiba, Japan. Hepatology 1989;10(6):998-1002. 19. Liu S, Chan KW, Wang B, et al. Fibrolamellar hepatocellular carcinoma. Am J Gastroenterol 2009;104(10):2617-24 [quiz 25]. 20. Kim KA, Kim KW, Park SH, et al. Unusual mesenchymal liver tumors in adults: Radiologic-pathologic correlation. Am J Roentgenol 2006;187(5):W481-9. 21. Peterson MS, Baron RL, Rankin SC. Hepatic angiosarcoma: Findings on multiphasic contrast-enhanced helical CT do not mimic hepatic hemangioma. Am J Roentgenol 2000; 175:165-70. 22. Bozaci EA, Taskin S, Gurkan O, et al. Intracavitary cardiac metastasis and pulmonary tumor emboli of choriocarcinoma: The first case diagnosed and treated without surgical intervention. Gynecol Oncol 2005;99(3):753-6. 23. Gonzalez-Vitale JC, Garcia-Bunuel R. Pulmonary tumor emboli and cor pulmonale in primary carcinoma of the lung. Cancer 1976;38(5):2105-10.
Curr Probl Diagn Radiol, July/August 2014
24. Kane RD, Hawkins HK, Miller JA, et al. Microscopic pulmonary tumor emboli associated with dyspnea. Cancer 1975;36(4):1473-82. 25. Rees H, Ang LC. Massive pulmonary tumor emboli in a sarcoma. An unusual cause of sudden death. Am J Forensic Med Pathol 1996;17(2):146-50.
Curr Probl Diagn Radiol, July/August 2014
26. Wakasa K, Sakurai M, Uchida A, et al. Massive pulmonary tumor emboli in osteosarcoma. Occult and fatal complication. Cancer 1990;66(3):583-6. 27. Whyte RI, Starkey TD, Orringer MB. Tumor emboli from lung neoplasms involving the pulmonary vein. J Thorac Cardiovasc Surg 1992;104(2):421-5.
231
Tumoral pulmonary emboli from hepatocellular carcinoma (HCC) have rarely been described, although invasion of the portal and hepatic venous systems is a well-known complication. HCC originating in a noncirrhotic liver in the absence of chronic hepatitis B infection is also uncommon. We present a case of a patient with chronic hepatitis C infection without hepatic cirrhosis who developed angioinvasive HCC with intracardiac extension and tumoral pulmonary emboli. Differential considerations, including combined HCC-cholangiocarcinoma, other hepatic mesenchymal tumors, and metastasis, are discussed. Owing to poor prognosis, no resection was attempted. Autopsy was performed because of the unusual clinical presentation, and immunohistochemistry of the hepatic tumor, the intracardiac extension, and the pulmonary emboli were concordant with hepatocellular origin. Even though definitive diagnosis may not affect patient outcome, it is important for radiologists and clinicians to be aware that angioinvasive HCC may arise in the absence of cirrhosis.
Introduction Hepatocellular carcinoma (HCC) includes most primary liver cancers. Rates of mortality and ageadjusted incidence have been documented in large series to be rising since 1976. There is higher incidence and mortality of HCC in men than in women and in black individuals as compared with white individuals. There is also increased incidence with age, with peak incidence among white men at approximately the age of 75 years.1 Prognostic factors From the aDepartment of Radiology, University of Washington, Seattle, WA; and bVA Puget Sound Health Care System, Seattle, WA. Reprint requests: Toshimasa Clark, MD, Department of Radiology, University of Washington, 1959 NE Pacific St, Box 357115, Seattle, WA 98195. E-mail: [email protected]. Curr Probl Diagn Radiol 2014;43:227–231. Published by Mosby, Inc. 0363-0188/$36.00 + 0 http://dx.doi.org/10.1067/j.cpradiol.2014.04.006
Curr Probl Diagn Radiol, July/August 2014
include age, presence of cirrhosis, tumor size, and adjuvant chemotherapy if resected.2 Imaging features characteristic for conventional HCC are as defined on the American College of Radiology's Liver Imaging and Reporting System, namely late arterial phase hyperenhancement, delayed phase hypoenhancement relative to liver parenchyma, and a delayed phase enhancing peripheral pseudocapsule.3 There exist well-defined, algorithmic imaging criteria such that categorization of observations into strata ranked by their probability of representing HCC is possible in a semiautomated fashion.4 Invasion of the portal and hepatic venous systems is a well-described finding seen in HCC, although extension into the inferior vena cava and right atrium is rare.5,6 The longest reported survival time for a patient with HCC with cardiac extension is 26 months.7 The surgical technique for resection of tumor with cardiac extension involves cardiopulmonary bypass, which may represent an unacceptable risk given the data indicating little potentially low long-term benefit. Treatment options for HCC include resection when surgically feasible, transplant, systemic chemotherapy, and locoregional therapies, including radiofrequency ablation, cryoablation, Yttrium-90 chemoembolization, and irreversible electroporation.8-11 Here, the authors present a case of HCC arising in a patient without hepatic cirrhosis, with the rare disease manifestations of both proven intracardiac extension and tumoral pulmonary emboli. In addition to the unusual clinical presentation, the imaging findings were atypical for HCC. Differential considerations included combined HCC-cholangiocarcinoma (HCC-CC), other hepatic mesenchymal tumors, and metastasis.
Methods This study was approved by our institutional review board. Computed tomography (CT) images with
227
FIG 1. Axial contrast-enhanced CT demonstrates a 7-cm mass in the Couinaud segment 7 that is hypervascular during the late arterial phase (left panel; arrow) and isodense without washout on delayed imaging (right panel; arrowhead).
intravenous contrast were acquired in late arterial, portal venous, and 5-minute delayed phases on an HD 750 64-slice scanner (GE Healthcare; Little Chalfont, Buckinghamshire, United Kingdom). Gross pathologic photography was performed with a 5D Mark II camera body and 24-105 mm f/4L IS lens (Canon, Inc; Tokyo, Japan), with postprocessing performed in Lightroom (Adobe, Inc; San Jose, CA). The clinical notes, laboratory data, and autopsy report were accessed through our institution's electronic medical record.
Case Report Our patient was a 65-year-old man with a history of chronic hepatitis C without hepatic cirrhosis who presented with 1 week of increased dyspnea on exertion, periumbilical abdominal pain, and malaise, following 6 months of similar, progressive symptoms. Right upper quadrant US demonstrated a thrombus within the inferior vena cava. A multiphase liverprotocol contrast-enhanced abdominal CT was subsequently performed. CT scan of the liver demonstrated a noncirrhotic liver morphology. There was a 7-cm infiltrative, arterially enhancing mass in the Couinaud hepatic segment 7 that became isodense on delayed phase imaging (Fig 1), without unequivocal washout relative to adjacent hepatic parenchyma. Enhancing thrombus was present with both a striated appearance and “thread-and-streak sign,” with extension into the hepatic veins, inferior vena cava,
228
and right atrium (Fig 2). The right atrium was nearly occluded by this thrombus. Owing to the extensive vascular invasion and near occlusion of the right atrium by presumed tumor thrombus, multidisciplinary assessment was that chemotherapeutic or surgical intervention would not prolong survival or palliate the patient's condition. The patient was placed on comfort care measures and died on the fourth hospital day with respiratory failure and asystole secondary to lactic acidosis. Test for alphafetoprotein level was incomplete, pending processing by the laboratory before the patient's death, and further laboratory assessment was halted at that point. Autopsy was performed, confirming the infiltrative hepatic mass as angioinvasive HCC arising in a noncirrhotic liver (Fig 3). There was tumoral
FIG 2. Coronal reformatted image from late arterial phase contrastenhanced CT demonstrates tumoral thrombus from HCC extending into the hepatic veins, inferior vena cava, and right atrium (arrow).
Curr Probl Diagn Radiol, July/August 2014
FIG 3. Sectioned liver from autopsy demonstrates primary HCC within right hepatic lobe (arrow) as well as HCC tumor thrombus within hepatic veins (arrowhead). Note the pathologic “thread-andstreak sign” and striated appearance of the tumor thrombus. (Color version of figure is available online.)
extension of HCC into the hepatic veins, inferior vena cava, and right atrium (Figs 3 and 4). The lungs were sectioned to assess the cause of the patient's respiratory failure. The large right atrial tumor thrombus and multiple pulmonary emboli were confirmed to be of HCC origin (Figs 4 and 5).
Discussion The main differential diagnoses considered in this case included HCC, combined HCC-CC, other primary hepatic mesenchymal tumors, and hypervascular metastases.8,12-15 In this case, HCC was suspected, although the patient did not have hepatic cirrhosis. Definitive diagnosis of HCC was confirmed at autopsy.
FIG 4. Heart seen at autopsy demonstrates a large HCC tumor thrombus adherent to the wall of the right atrium (arrow). (Color version of figure is available online.)
Curr Probl Diagn Radiol, July/August 2014
FIG 5. Sectioned lung at autopsy demonstrates HCC tumoral emboli within multiple pulmonary arteries (arrows). (Color version of figure is available online.)
When HCC arises in patients without cirrhosis, data from small series suggest that it does so at a younger age, is more common in women, and is less likely to be associated with elevated alpha-fetoprotein.16 These demographic characteristics may be region dependent, as another series of patients seen at the University of Pittsburgh who developed HCC in the absence of hepatic cirrhosis demonstrated a male predominance and wide age range.17 The incidence of HCC arising in cirrhotic vs noncirrhotic livers also demonstrates geographical variation, with Tiribelli et al reporting that 87% of cases of HCC in Trieste, Italy, and 81% of cases of HCC in Chiba, Japan, arose in patients with underlying hepatic cirrhosis.18 Fibrolamellar HCC typically arises in younger patients without hepatic cirrhosis. Characteristic imaging features include arterial hyperenhancement and a hypodense, T2hypointense central scar, often with calcification.19 In this case, imaging findings and patient demographics were inconsistent with fibrolamellar HCC, although hepatic cirrhosis was absent. HCC-CC has been reported to have imaging features that overlap with those of HCC and cholangiocarcinoma, which may reflect origin from a common progenitor cell. Reported sensitivity and accuracy of imaging is low, with Fowler et al13 reporting sensitivities and specificities of 33%-34% and 81%-100% for 2 readers. In this case, although the imaging features of the primary hepatic lesion and tumoral thrombus were not classic for HCC, they were not typical for cholangiocarcinoma either, with a lack of progressive delayed enhancement. Metastases to the liver are typically hypovascular. As per a large series conducted by Danet et al,14
229
hypervascular metastases typically show peripheral enhancement in the arterial phase, with adjacent hypoenhancement and central progressive enhancement during the delayed phase. Primary malignancies associated with a higher incidence of hypervascular metastases include breast carcinoma, carcinoid, neuroendocrine tumor, renal cell carcinoma, and thyroid carcinoma.14,15 Other tumors may arise from the mesenchymal cells of the liver and demonstrate a diverse set of imaging features. Angiosarcoma is the primary differential consideration among these given imaging findings of arterial phase hyperenhancement. The classic history of distant prior exposure to Thorotrast contrast is now seen in a minority of patients found to have hepatic angiosarcoma, and its imaging appearance varies from a solid mass with progressive enhancement to a predominantly cystic lesion with only peripheral enhancement.12,20,21 The appearance of the hepatic angioinvasive mass in this case was not incompatible with angiosarcoma, but there were no imaging features suggesting this diagnosis specifically. This case represents an instance of angioinvasive HCC arising in a noncirrhotic liver, the incidence of demonstrates geographical variability. Documentation of pathology-proven tumoral emboli to the pulmonary arteries from HCC is exceptionally rare, with prior reports of tumoral emboli arising from sarcomas, germ cell tumors, and carcinomas of the prostate, breast, stomach, pancreas, and liver.22-27 It is important for radiologists and clinicians to be aware that angioinvasive HCC may arise in the absence of cirrhosis, even though definitive diagnosis may not affect patient outcome if the patient presents at an advanced stage of disease, such as in the case of our patient.
REFERENCES 1. El-Serag HB, Mason AC. Rising incidence of hepatocellular carcinoma in the United States. N Engl J Med 1999;340 (10):745-50. 2. Nagasue N, Kohno H, Chang Y, et al. Liver resection for hepatocellular carcinoma: results of 229 consecutive patients during 11 years. Ann Surg 1993;217(4):375-84. 3. Radiology ACo. Liver imaging reporting and data system version 2013.1, 2013. 4. Clark TJ, McNeeley MF, Maki JH. Design and implementation of handheld and desktop software for the structured reporting of hepatic masses using the LI-RADS schema. Acad Radiol 2014;21(4):491-506. 5. McBride K, Masterson J. The thread and streak sign of portal vein tumour thrombus demonstrated by colour Doppler imaging. Br J Radiol 1992;65(775):607-9.
230
6. Raab BW. The thread and streak sign. Radiology 2005;236 (1):284-5. 7. Wu CC, Hseih S, Ho W, et al. Surgical treatment for recurrent hepatocellular carcinoma with tumor thrombi in right atrium: Using cardiopulmonary bypass and deep hypothermic circulatory arrest. J Surg Oncol 2000;74:227-31. 8. Ryder SD. Guidelines for the diagnosis and treatment of hepatocellular carcinoma (HCC) in adults. Gut 2003; 52(suppl III):iii1-8. 9. Lu DS, Yu NC, Raman SS, et al. Radiofrequency ablation of hepatocellular carcinoma: Treatment success as defined by histologic examination of the explanted liver. Radiology 2005;234:954-60. 10. Bhargava P, Vaidya S, Dick AA, et al. Imaging of orthotopic liver transplantation: Review. Am J Roentgenol 2011;196 (suppl 3):WS15-25 [Quiz S35-8]. 11. Shin DS, Dighe MK, Wang C, et al. Surgical resection of a malignant liver lesion: What the surgeon wants the radiologist to know. Am J Roentgenol, in press. 12. Bhargava P, Iyer RS, Moshiri M, et al. Radiologic-pathologic correlation of uncommon mesenchymal liver tumors. Curr Prob Diagn Radiol 2013;42(5):183-90. 13. Fowler KJ, Sheybani A, Parker RA 3rd, et al. Combined hepatocellular and cholangiocarcinoma (biphenotypic) tumors: Imaging features and diagnostic accuracy of contrast-enhanced CT and MRI. Am J Roentgenol 2013;201(2):332-9. 14. Danet IM, Semelka RC, Leonardou P, et al. Spectrum of MRI appearances of untreated metastases of the liver. Am J Roentgenol 2003;181:809-17. 15. Sica GT, Hoon Ji, Ros PR. CT and MR imaging of hepatic metastases. Am J Roentgenol 2000;174:691-8. 16. Melia WM, Wilkinson ML, Portmann BC, et al. Hepatocellular carcinoma in the non-cirrhotic liver: A comparison with that complicating cirrhosis. Q J Med 1984;53(211):391-400. 17. Brancatelli G, Federle MP, Grazioli L, et al. Hepatocellular carcinoma in noncirrhotic liver: CT, clinical, and pathologic findings in 39 U.S. residents. Radiology 2002;222(1):89-94. 18. Tiribelli C, Melato M, Croce LS, et al. Prevalence of hepatocellular carcinoma and relation to cirrhosis: Comparison of two different cities of the world—Trieste, Italy, and Chiba, Japan. Hepatology 1989;10(6):998-1002. 19. Liu S, Chan KW, Wang B, et al. Fibrolamellar hepatocellular carcinoma. Am J Gastroenterol 2009;104(10):2617-24 [quiz 25]. 20. Kim KA, Kim KW, Park SH, et al. Unusual mesenchymal liver tumors in adults: Radiologic-pathologic correlation. Am J Roentgenol 2006;187(5):W481-9. 21. Peterson MS, Baron RL, Rankin SC. Hepatic angiosarcoma: Findings on multiphasic contrast-enhanced helical CT do not mimic hepatic hemangioma. Am J Roentgenol 2000; 175:165-70. 22. Bozaci EA, Taskin S, Gurkan O, et al. Intracavitary cardiac metastasis and pulmonary tumor emboli of choriocarcinoma: The first case diagnosed and treated without surgical intervention. Gynecol Oncol 2005;99(3):753-6. 23. Gonzalez-Vitale JC, Garcia-Bunuel R. Pulmonary tumor emboli and cor pulmonale in primary carcinoma of the lung. Cancer 1976;38(5):2105-10.
Curr Probl Diagn Radiol, July/August 2014
24. Kane RD, Hawkins HK, Miller JA, et al. Microscopic pulmonary tumor emboli associated with dyspnea. Cancer 1975;36(4):1473-82. 25. Rees H, Ang LC. Massive pulmonary tumor emboli in a sarcoma. An unusual cause of sudden death. Am J Forensic Med Pathol 1996;17(2):146-50.
Curr Probl Diagn Radiol, July/August 2014
26. Wakasa K, Sakurai M, Uchida A, et al. Massive pulmonary tumor emboli in osteosarcoma. Occult and fatal complication. Cancer 1990;66(3):583-6. 27. Whyte RI, Starkey TD, Orringer MB. Tumor emboli from lung neoplasms involving the pulmonary vein. J Thorac Cardiovasc Surg 1992;104(2):421-5.
231