Published online before print January 18, 2002, 10.1148/radiol.2223010030
(Radiology 2002;222:693-698.)
© RSNA, 2002
Angiographic Classification of Hepatic Hemangiomas in Infants1
Ara Kassarjian, MD,
Josée Dubois, MD and
Patricia E. Burrows, MD
1 From the Department of Radiology, Children’s Hospital, Boston, Mass (A.K., P.E.B.); and Department of Medical Imaging, Hôpital Sainte-Justine, Montreal, Quebec, Canada (J.D.). From the 2000 RSNA scientific assembly. Received November 27, 2000; revision requested January 11, 2001; final revision received June 29; accepted July 18. Address correspondence to A.K., Department of Radiology, Boston University School of Medicine, Boston Medical Center, One Boston Medical Center Pl, Boston, MA 02118 (e-mail: akassarjian@hotmail.com).
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ABSTRACT
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PURPOSE: To review the angiograms in patients with hepatic hemangiomas referred to two North American children’s hospitals to determine the variability in angiographic findings and to propose a classification system that is based on these findings.
MATERIALS AND METHODS: Angiograms obtained in 15 infants with a diagnosis of hepatic hemangioma who were examined at or referred to two tertiary pediatric hospitals in North America from 1981 through 2000 were reviewed. The angiographic findings were then used to classify hemangiomas into types on the basis of a number of features, including high-flow nodules, early filling of veins, and the type of direct shunt present. Clinical data, including age at presentation, presence of cardiac insufficiency, and treatment, were also recorded.
RESULTS: Lesions were classified into five types on the basis of angiographic findings. In three of 15 patients, angiograms demonstrated the classic appearance of hepatic hemangiomas, with early filling of abnormal vascular channels, stagnation of contrast material, and no evidence of a direct shunt (type 1). In four patients, images showed high-flow nodules without direct shunts (type 2). In eight patients, direct shunts were demonstrated: arteriovenous shunts (type 3) in one, portovenous shunts (type 4) in three, and both arteriovenous and portovenous shunts (type 5) in four.
CONCLUSION: Hepatic hemangioma in infants is a heterogeneous lesion with variable angioarchitecture and a spectrum of angiographic findings.
© RSNA, 2002
Index terms: Angioma, 761.3194 • Liver neoplasms, angiography, 761.124 • Liver neoplasms, in infants and children, 761.3194
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INTRODUCTION
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Hepatic hemangioma is the most common hepatic neoplasm in infants (1). Though these lesions usually are asymptomatic and are found incidentally during imaging for other indications, some are associated with symptoms on the basis of their size, location, hemodynamics, or hematologic effects. Patients with atypical hepatic hemangiomas often are referred to a tertiary care facility for confirmation of diagnosis and selection of appropriate treatment.
Although hepatic hemangiomas are common, they are a heterogeneous group of lesions that may resemble other vascular lesions (2). Atypical hepatic hemangiomas are sometimes mistaken for vascular malformations or malignant neoplasms and vice versa. It is crucial to distinguish hemangiomas from these other lesions because the natural history of and appropriate therapy for these lesions differ dramatically. Vascular malformations are present at birth and grow proportionally with the child. They do not regress spontaneously, nor do they respond to medical therapy (3,4).
In contradistinction, hemangiomas are benign neoplasms that have an early proliferative phase and a subsequent phase of involution. Hemangiomas respond to therapy with steroids or interferon alpha-2a, although results of a prospective randomized trial in which the effectiveness of interferon is evaluated has not yet been published (5–7). In rare cases, hemangiomas are refractory to medical therapy and require embolization or surgery. However, in some patients, embolization is ineffective or is associated with hepatic necrosis or sepsis (8,9). Differences in angioarchitecture may possibly account for the variability in clinical presentation and in results of embolization.
The purpose of our study was to review the angiograms obtained in infants with hepatic hemangiomas who were referred to two North American children’s hospitals to determine the variability in angiographic findings and to propose a classification system that is based on these angiographic findings.
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MATERIALS AND METHODS
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The radiology and the Vascular Anomalies Center databases at two tertiary children’s hospitals were searched from 1981 through 2000 for reports containing the keywords liver or hepatic and hemangioma. Of patients who met these criteria, 62 had hepatic hemangiomas. Institutional review board approval or informed consent for database searches were not required in our institutions.
Angiograms were obtained in 15 of 62 patients with liver hemangiomas. All 15 patients also underwent additional imaging studies, including ultrasonography (US) (12 patients), computed tomography (CT) (10 patients), and/or magnetic resonance (MR) imaging (six patients). In the remaining 47 patients, angiograms were not obtained, and these patients were excluded from the study. In the 15 patients in our study, the diagnosis was based on pathologic findings (four patients), response to therapy (seven patients), or classic imaging findings with (three patients) or without (one patient) associated cutaneous hemangiomas. Classic imaging findings included focal or multifocal mass lesions that were hyperintense on T2-weighted MR images, that had centripetal enhancement on contrast material–enhanced CT scans or MR images, and that demonstrated enlarged feeding arteries with or without large draining veins (2,4,5,7).
Two radiologists (A.K., P.E.B.) jointly reviewed the angiograms in conjunction with images from any other available studies and then characterized the angiograms according to the number of lesions (single or multiple), flow characteristics (high vs low on the basis of the angiographic enhancement pattern), presence and type of a shunt (arteriovenous, arterioportal, portovenous), and major anomalies of hepatic vessels (particularly venous varices). Clinical information regarding the age at presentation, sex, presence of congestive heart failure (CHF), treatment, and other pertinent findings were recorded. Pathologic findings, when available, were reviewed. Angiograms were then classified by the two radiologists together on the basis of the presence of high-flow nodules (focal rapid collections of contrast material), the early filling of veins, and the type of direct macroscopic shunt present.
The angiographic techniques varied slightly on the basis of available equipment and local expertise. All patients underwent injection of the aorta and hepatic arteries and selective injections of large arteries, including intercostal and phrenic arteries, supplying the hemangiomas. Evaluation of the portal venous system by means of either direct injection or delayed images following selective superior mesenteric artery (SMA) injection were inconsistent. The amount of intravenous contrast material used varied widely (5–10 mL/kg of contrast material with an iodine concentration of 240 mg/mL), depending on the number of lesions, the vascular supply to the lesions, and the number and diameter of vessels that were embolized. Embolization was performed with a variety of materials, including platinum-and-fiber microcoils, polyvinyl alcohol foam particles, and cyanoacrylic polymer. Portovenous shunts were embolized with coils.
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RESULTS
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On the basis of our review of the angiograms, we were able to classify lesions into five types (Table 1). Type 1 lesions were the classic hemangiomas with early filling of abnormal vascular channels and with stagnation and pooling of contrast material. Type 1 lesions did not have any early filling of hepatic veins or an arteriovenous or portovenous shunt. Type 2 lesions contained focal high-flow nodules with early filling of veins and with no visible direct shunts. Type 1 and 2 lesions did not contain any major vascular anomalies. Type 3 lesions contained angiographically visible direct arteriovenous (including arterioportal) shunts, whereas type 4 lesions contained direct portovenous shunts. Type 5 lesions contained both direct arteriovenous and portovenous shunts.
Of the 15 patients in whom angiograms were obtained, three had type 1 hemangiomas (Fig 1). There was no evidence of an arteriovenous or portovenous shunt. All these lesions had low flow. The mean age at presentation was 16 days (age range, 1–60 days) (Table 2). None of these patients had CHF, although one had respiratory distress probably caused by the mass effect of the enlarged liver. One of these patients had a single large hemangioma and persistent neonatal anemia. He was treated with blood transfusions but never received any direct treatment for the hemangioma. He died of sudden infant death syndrome at home. Postmortem examination findings confirmed the presence of a large vascular thrombus in a hepatic hemangioma. Another patient with a single type 1 lesion responded to therapy with interferon alpha-2a. The patient in whom medical therapy (steroids and interferon) failed and who was treated with embolization had multifocal lesions. This patient had regression of the hemangioma and the symptoms.
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Figure 1a. Frontal conventional angiograms of a type 1 liver hemangioma. (a) Image obtained after injection of the celiac artery in a 1-month-old boy demonstrates early filling of abnormal vascular channels (arrows) without evidence of enhancing nodules or a direct shunt. (b) Delayed image from the same angiogram demonstrates stagnation of contrast material in the liver lesion. In this patient, postmortem examination findings confirmed the presence of a thrombus in the center of the lesion.
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Figure 1b. Frontal conventional angiograms of a type 1 liver hemangioma. (a) Image obtained after injection of the celiac artery in a 1-month-old boy demonstrates early filling of abnormal vascular channels (arrows) without evidence of enhancing nodules or a direct shunt. (b) Delayed image from the same angiogram demonstrates stagnation of contrast material in the liver lesion. In this patient, postmortem examination findings confirmed the presence of a thrombus in the center of the lesion.
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In four patients, angiograms demonstrated multiple lesions with high-flow nodules and early filling of veins without any visible direct shunt (type 2) (Fig 2). All four patients were younger than 2 months of age at presentation, and the mean age was 21 days (median age, 16 days). Because of CHF and the inability to achieve adequate control of the condition with therapy with steroids and interferon, all four of these patients underwent embolization. One patient also had severe primary hypothyroidism and diffuse hemangiomatosis of the liver (innumerable hemangiomas involving the entire liver) and the skin. In this patient, CHF was likely related to hypothyroidism because there were no visible direct shunts in the lesion, and the hepatic veins were not dilated. Despite multimodality treatment, including radiation therapy and abdominal fasciotomy, he died. Autopsy findings confirmed the presence of diffuse hepatic involvement with hemangiomas.
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Figure 2a. Frontal digital subtraction angiograms of type 2 liver hemangiomas in a newborn boy with respiratory distress. (a) Image obtained during the portal venous phase demonstrates multiple high-flow nodules (arrows) being fed by portal vein branches. There is no evidence of direct shunts. (b) Image obtained during the hepatic arterial phase shows no evidence of shunts and demonstrates that the lesions in this patient are not supplied by branches of the hepatic artery. (c) Image obtained during the parenchymal phase after injection of the hepatic artery demonstrates a "negative" image of the multiple liver lesions, which appear as filling defects (arrows).
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Figure 2b. Frontal digital subtraction angiograms of type 2 liver hemangiomas in a newborn boy with respiratory distress. (a) Image obtained during the portal venous phase demonstrates multiple high-flow nodules (arrows) being fed by portal vein branches. There is no evidence of direct shunts. (b) Image obtained during the hepatic arterial phase shows no evidence of shunts and demonstrates that the lesions in this patient are not supplied by branches of the hepatic artery. (c) Image obtained during the parenchymal phase after injection of the hepatic artery demonstrates a "negative" image of the multiple liver lesions, which appear as filling defects (arrows).
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Figure 2c. Frontal digital subtraction angiograms of type 2 liver hemangiomas in a newborn boy with respiratory distress. (a) Image obtained during the portal venous phase demonstrates multiple high-flow nodules (arrows) being fed by portal vein branches. There is no evidence of direct shunts. (b) Image obtained during the hepatic arterial phase shows no evidence of shunts and demonstrates that the lesions in this patient are not supplied by branches of the hepatic artery. (c) Image obtained during the parenchymal phase after injection of the hepatic artery demonstrates a "negative" image of the multiple liver lesions, which appear as filling defects (arrows).
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Another patient with type 2 hemangioma who also manifested this condition at birth had severe CHF and renal and hepatic insufficiency and did not respond to treatment with steroids or embolization. Despite aggressive multimodality therapy, including radiation therapy, he died at the age of 7 days owing to hemorrhagic shock and disseminated intravascular coagulation. The other two patients responded to embolization, with subsequent resolution of respiratory and cardiac symptoms and a decrease in the size of the hemangiomas.
The patient with a type 3 lesion manifested this condition at 4 days old, with CHF and hepatomegaly (Fig 3). He had a focal hemangioma with a direct arterioportal shunt and a patent ductus venosus, which resulted in an arteriovenous shunt and a high-output state. There was also tapering of the aorta distal to the SMA. He was initially treated with steroids and then interferon. However, CHF persisted, and he was treated with embolization, with almost immediate resolution of CHF. Interferon therapy was continued until complete regression of the hemangioma was confirmed with MR imaging findings.
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Figure 3a. Frontal digital subtraction angiograms of type 3 liver hemangioma in a 4-day-old boy with CHF. (a) Image obtained after injection of the phrenic artery demonstrates abnormal vessels that supply a large hemangioma (straight arrow) in the right lobe of the liver and an intralesional shunt to the portal vein (curved arrow). (b) Image obtained after injection of the aorta demonstrates tapering of the aorta (arrow) just distal to the takeoff of the large arteries that supply the hemangioma. Image (not shown) obtained after injection of intercostal artery demonstrated a direct shunt from the intercostal artery to the right portal vein.
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Figure 3b. Frontal digital subtraction angiograms of type 3 liver hemangioma in a 4-day-old boy with CHF. (a) Image obtained after injection of the phrenic artery demonstrates abnormal vessels that supply a large hemangioma (straight arrow) in the right lobe of the liver and an intralesional shunt to the portal vein (curved arrow). (b) Image obtained after injection of the aorta demonstrates tapering of the aorta (arrow) just distal to the takeoff of the large arteries that supply the hemangioma. Image (not shown) obtained after injection of intercostal artery demonstrated a direct shunt from the intercostal artery to the right portal vein.
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Three patients with type 4 lesions manifested this condition within 2 months of age (median age, 14 days), and they had CHF and multiple liver lesions. In all three, pharmacologic treatment failed, and angiography and embolization (Fig 4) were performed. Angiographic findings demonstrated the presence of an extensive portovenous shunt within the lesions in addition to supply from hepatic arteries and adjacent systemic collateral vessels. Although these patients eventually responded to embolization, they required multiple sessions of embolization and had a protracted clinical course compared with other patients.
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Figure 4. Frontal digital subtraction angiogram of type 4 liver hemangioma in a 2-month-old girl with CHF. Image obtained after transhepatic injection of the left portal vein demonstrates portal vein branches that supply a hemangioma in the left lobe of the liver. There is a direct shunt from the portal vein (curved arrow) to a hepatic vein (straight arrow).
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Four patients with type 5 lesions manifested CHF within the 1st month of life, with three of four manifesting this condition within the first 2 days of life. One patient had multifocal lesions, whereas the other three had focal single lesions (Figs 5, 6). All four patients had CHF, which was refractory to pharmacologic therapy, and they required embolization. All four patients responded very quickly to embolization, which controlled the CHF.
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Figure 5a. Frontal digital subtraction angiograms of a type 5 liver hemangioma in a 1-day-old girl with CHF. (a) Image obtained after injection of the SMA demonstrates two lesions (curved arrows) in the right lobe of the liver. There is evidence of a shunt with early opacification of the portal vein (straight arrow). (b) Delayed image obtained after injection of the SMA demonstrates pooling of contrast material in the lesions. Note the direct shunt from the portal vein to the hepatic vein (arrow). Postembolization frontal image (not shown) obtained after injection of the left portal vein demonstrated persistent portovenous shunts after a catheter was passed from the middle hepatic vein through a shunt into the left portal vein.
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Figure 5b. Frontal digital subtraction angiograms of a type 5 liver hemangioma in a 1-day-old girl with CHF. (a) Image obtained after injection of the SMA demonstrates two lesions (curved arrows) in the right lobe of the liver. There is evidence of a shunt with early opacification of the portal vein (straight arrow). (b) Delayed image obtained after injection of the SMA demonstrates pooling of contrast material in the lesions. Note the direct shunt from the portal vein to the hepatic vein (arrow). Postembolization frontal image (not shown) obtained after injection of the left portal vein demonstrated persistent portovenous shunts after a catheter was passed from the middle hepatic vein through a shunt into the left portal vein.
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Figure 6a. Frontal digital subtraction angiograms of a type 5 liver hemangioma in a 2-day-old boy. (a) Image obtained after injection of the aorta demonstrates abnormal intercostal arteries (straight arrow) and phrenic arteries (curved arrow) that supply a focal liver hemangioma. (b) Delayed image after injection of the SMA demonstrates a direct shunt from the portal vein to a hepatic vein (curved arrow). The truncated appearance of the left portal vein (straight arrow) suggests a portal venous supply to a hemangioma in the left lobe of the liver. (c) Delayed image after injection of the aorta demonstrates a large varix (arrow) in the left lobe of the liver with dilated tortuous veins (arrowhead) draining the central varix. (Figures 6a and Figures 6c reprinted, with permission, from reference 10.)
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Figure 6b. Frontal digital subtraction angiograms of a type 5 liver hemangioma in a 2-day-old boy. (a) Image obtained after injection of the aorta demonstrates abnormal intercostal arteries (straight arrow) and phrenic arteries (curved arrow) that supply a focal liver hemangioma. (b) Delayed image after injection of the SMA demonstrates a direct shunt from the portal vein to a hepatic vein (curved arrow). The truncated appearance of the left portal vein (straight arrow) suggests a portal venous supply to a hemangioma in the left lobe of the liver. (c) Delayed image after injection of the aorta demonstrates a large varix (arrow) in the left lobe of the liver with dilated tortuous veins (arrowhead) draining the central varix. (Figures 6a and Figures 6c reprinted, with permission, from reference 10.)
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Figure 6c. Frontal digital subtraction angiograms of a type 5 liver hemangioma in a 2-day-old boy. (a) Image obtained after injection of the aorta demonstrates abnormal intercostal arteries (straight arrow) and phrenic arteries (curved arrow) that supply a focal liver hemangioma. (b) Delayed image after injection of the SMA demonstrates a direct shunt from the portal vein to a hepatic vein (curved arrow). The truncated appearance of the left portal vein (straight arrow) suggests a portal venous supply to a hemangioma in the left lobe of the liver. (c) Delayed image after injection of the aorta demonstrates a large varix (arrow) in the left lobe of the liver with dilated tortuous veins (arrowhead) draining the central varix. (Figures 6a and Figures 6c reprinted, with permission, from reference 10.)
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Four patients who had focal lesions that contained either a direct arteriovenous shunt or a portovenous shunt (two with type 4 and two with type 5 lesions) had hemangiomas that contained a large central varix (Fig 6c). Multiple feeding vessels drained into this large varix, which subsequently drained into circumferential hepatic veins. This type of angioarchitecture was not seen in patients with diffuse or multifocal hemangiomas or in those whose lesions did not contain direct shunts. Patients whose lesions contained a large central varix responded rapidly to embolization.
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DISCUSSION
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Although most hepatic hemangiomas in infants are asymptomatic lesions, a subgroup may be associated with symptoms on the basis of their size, location, and hemodynamics. We, therefore, propose a classification system that is based on the variable angioarchitecture of hepatic hemangiomas and demonstrate that direct arteriovenous, arterioportal, and portovenous shunts may be seen in hemangiomas. Although a microscopic intralesional shunt is a known feature of hepatic hemangiomas, we demonstrate that there can be a direct macroscopic, angiographically visible arteriovenous and portovenous shunt. In addition, we demonstrate that a shunt may be from arterial feeding vessels to the portal vein. Finally, we describe a central varix that may be seen in hemangiomas that contain direct shunts (types 4 and 5). Knowledge of this variability in angioarchitecture is potentially important, since it may help prevent misdiagnosis of hemangiomas as other vascular anomalies, especially arteriovenous malformations. Accurate diagnosis is critical in planning treatment in these patients.
Although imaging of hemangiomas usually is performed with cross-sectional techniques, such as US, CT, or MR imaging, knowledge of the varying angioarchitecture is extremely useful when interpreting findings in these studies and when planning endovascular therapy (9,11). As we gain more experience with different types of noninvasive vascular imaging, this classification system may potentially be extrapolated to other imaging modalities. For example, since some hemangiomas can be detected with antenatal US, the observations reported in this study can be used to determine the diagnosis and to predict the need for postnatal treatment. One such patient, whose type 5 hemangioma was detected at 28 weeks gestation, was successfully treated in utero with administration of corticosteroids to the mother, with a good outcome (12). At our institution, angiography is performed only with the intent of proceeding with endovascular therapy to control the patient’s symptoms. The main indication for embolization is high-output cardiac failure that is refractory to pharmacologic therapy.
In our series, patients who had focal lesions with a direct shunt (ie, types 3, 4, or 5) usually had CHF either at or shortly after birth. In these patients, the CHF was secondary to the direct shunts, which were often accessible to a catheter. In these patients, CHF responded very quickly to embolization of the shunts, with the patients being extubated and stable usually within a day. We believe early embolization is indicated in patients with focal lesions and a direct shunt, since it seems to quickly and effectively control the CHF.
Patients whose hemangiomas had an extensive portal venous supply were more difficult to treat. Although embolization of the direct portovenous shunts resulted in some improvement in CHF, these patients often had comorbid conditions (eg, hypothyroidism) that likely contributed to the CHF. As such, these patients usually had a more protracted clinical course and required combined treatment strategies to control symptoms. The usefulness of portal embolization to treat these patients is not entirely clear, although it is known that patients with portovenous fistulas may develop fatal hepatic necrosis after embolization of the hepatic arteries alone (13).
One limitation of our study is that pathology records of findings used to confirm the diagnosis of hemangioma were only available in four patients. However, we believe that response to therapy (as seen in seven patients) and concomitant cutaneous hemangiomas (three patients), although not definitive, are strong evidence for the diagnosis in 10 of 11 patients for whom pathology reports were unavailable. Only one patient had a presumed diagnosis that was based solely on classic imaging findings. At the time of publication of this article, follow-up findings in this patient are not yet available.
The proposed classification system that is based on angiographic findings may aid in ensuring a degree of uniformity in studying hepatic hemangiomas such that as new treatment protocols are proposed, it may be easier to determine which type of therapy is most appropriate for each type, or subtype, of lesion.
In summary, we propose a classification system that is based on angiographic findings and that reflects the variability in the angioarchitecture of hepatic hemangiomas in infants. This classification system may help improve the accuracy of diagnosis of these lesions and may help in the determination of the most appropriate form of therapy and, when needed, aid in the planning of endovascular treatment.
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FOOTNOTES
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Abbreviations: CHF = congestive heart failure,
SMA = superior mesenteric artery
Author contributions: Guarantors of integrity of entire study, A.K., P.E.B.; study concepts and design, A.K., J.D., P.E.B.; literature research, A.K., P.E.B.; clinical studies, P.E.B., J.D.; data acquisition and analysis/interpretation, A.K., J.D., P.E.B.; manuscript preparation, A.K., P.E.B., J.D.; manuscript definition of intellectual content, editing, and revision/review, A.K., P.E.B.; manuscript final version approval, A.K., J.D., P.E.B.
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ABSTRACT
INTRODUCTION
