Hepatic Epithelioid Hemangioendothelioma: Resection or Transplantation, Which and When?
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1 Hepatic Epithelioid Hemangioendothelioma: Resection or Transplantation, Which and When? Menahem Ben-Haim,* Sasan Roayaie,* Ming Q. Ye, Swan N. Thung, Sukru Emre,* Thomas A. Fishbein,* Patricia M. Sheiner,* Charles M. Miller,* and Myron E. Schwartz* Hepatic epithelioid hemangioendothelioma (HEHE) is a rare tumor with an unpredictable course and prognosis. The aim of this study is to describe our experience with liver resection, as well as transplantation, in the treatment of this tumor. We retrospectively analyzed the clinical features, pathological findings, and postoperative results in a series of 11 patients presenting between 1990 and Five patients (45%) presented with abdominal pain, 3 patients (27%) with jaundice and ascites, and the rest were asymptomatic. Computed tomography or magnetic resonance imaging showed localized lesions in 2 patients (18%) and multifocal disease in the others. Seven patients (64%) had extrahepatic lesions, detected either by preoperative imaging or discovered at exploration. Two resections of apparently localized lesions were followed by rapid and aggressive recurrence. Five patients were treated with transplantation, including 1 patient who had previously undergone resection. Of these 5 patients, 2 patients are currently free of detectable disease, 1 patient who had severe ascites and jaundice is now asymptomatic with stable extrahepatic lesions, and 2 patients (including 1 who had previously undergone a resection) died of tumor recurrence. One patient with advanced tumor died while waiting for transplantation. The remaining 4 patients are free of symptoms and have stable hepatic and extrahepatic disease. HEHE is nearly always multifocal, and our results with resection were dismal. Because of the unpredictable nature of the tumor, the indications for transplantation in patients without liver-related symptoms should be carefully evaluated. Nevertheless, extrahepatic disease should not be an absolute contraindication for liver transplantation in patients with severe liver dysfunction. Copyright 1999 by the American Association for the Study of Liver Diseases From *The Recanati/Miller Transplantation Institute; and the Department of Pathology, The Mount Sinai Hospital of Mount Sinai New York University Medical Center and Health System, New York, NY. Address reprint requests to Myron E. Schwartz, MD, The Recanati/Miller Transplantation Institute, Mount Sinai Medical Center, Box 1104, One Gustave L. Levy Pl, New York, NY Copyright 1999 by the American Association for the Study of Liver Diseases /99/ $3.00/0 H epatic epithelioid hemangioendothelioma (HEHE) is a rare and unique vascular tumor, first defined as a specific entity by Weiss and Enzinger 1 in In 1975, Dail and Liebow 2 described a similar tumor in the lung, which they named intravascular bronchioalveolar tumor. The clinical presentation is variable, and the natural history of this tumor is unpredictable. It may be an incidental finding, or it may present with nonspecific or mild symptoms. 3-5 Nonetheless, it is usually multifocal, with evidence of extrahepatic disease at the time of diagnosis. 3-6 Findings of multiple peripheral hepatic lesions with capsular retraction on computed tomography (CT) or magnetic resonance imaging are highly suggestive of HEHE, 6,7 but the diagnosis should be confirmed by histopathological evaluation (Fig. 1) and positive immunostains for factor VIII or CD 34 antigens (Fig. 2). 4,8 Most investigators define HEHE as a low- to intermediate-grade malignancy, and there are reports of prolonged survival without treatment. 3-5 Most of the available literature on HEHE is composed of only case reports. 3 Ishak et al 4 published a series of 32 cases collected over 17 years, which was the first study to define the clinical and pathological characteristics of this tumor. Experience with medical treatment is very limited, with limited degrees of success reported with various modalities. 3,9,10 Since its application in the treatment of primary liver malignancies, orthotopic liver transplantation (OLT) has been considered the treatment of choice for HEHE and has been associated with reasonable results The inability to predict the behavior of this tumor, and therefore its prognosis, as well as the limited 526 Liver Transplantation and Surgery, Vol 5, No 6 (November), 1999: pp
2 Hepatic Epithelioid Hemangioendothelioma 527 quadrant abdominal pain, 3 patients with ascites and jaundice, 2 patients with elevated liver enzyme levels on routine screening, and 1 patient was evaluated for atypical chest pain. Imaging studies of the liver showed bilateral disease in 9 patients and disease localized in the right lobe in 2 patients. Three patients showed symptoms of hepatic vein occlusion. Initial metastatic workup was positive in 4 patients, with splenic lesions (2 patients), bone lesions (2 patients), lung lesions (2 patients), and retroperitoneal lymph node involvement (1 patient). Peritoneal spread was found during exploration in 2 additional patients, and in 1 patient, there was a direct invasion of the diaphragm. Figure 1. Tumor cells with epithelioid features in a portal vein branch (arrows). (Hematoxylin and eosin, original magnification 250.) availability of cadaveric livers, raises controversy over the indications, contraindications, and patient selection criteria for OLT in the treatment of HEHE. 14,15 Material and Methods Patient Profiles Between May 1990 and October 1998, 11 patients with HEHE were evaluated and treated at the Mount Sinai Medical Center (New York, NY). There were 7 men (mean age at diagnosis, 51 years; range, 34 to 69 years) and 4 women (mean age, 51 years; range, 25 to 77 years). We retrospectively reviewed their medical records, radiological studies, and pathological specimens. In all cases, the diagnosis was based on liver biopsy findings that met the morphological criteria described by Weiss and Enzinger 1 and the immunostaining criteria suggested by Ishak et al. 4 When patients were referred from other institutions, the hepatobiliary pathologist reviewed the specimens and confirmed the diagnosis. Treatment Two patients with lesions localized to the right lobe by preoperative imaging underwent primary right trisegmentectomy. In 1 patient, omentectomy, partial resection of the diaphragm, and excision of a small left lobe lesion were added to the resection. Preoperative portal vein embolization was performed in 1 patient. Five patients underwent OLT, including 1 patient who originally underwent a resection. Transplantation was performed in the standard fashion. Post-OLT immunosuppression consisted of prednisone and tacrolimus (4 patients) or prednisone and cyclosporine (1 patient). One posttransplantation patient with tumor recurrence in the right lobe was treated with a secondary right lobectomy. When peritoneal tumor deposits were found during laparotomy (2 patients), a peritoneal catheter was inserted, and the patients were treated with intraperitoneal 5-fluorouracil (Table 2). Four of the remaining 5 patients were evaluated for transplantation. The fifth patient was not a candidate for transplantation. Follow-Up A history, physical examination, complete blood workup, and abdominal imaging (CT or magnetic resonance imaging) were conducted every 3 to 6 months. Additional studies, including bone scans, chest CT, and Doppler ultrasonography, or diagnostic procedures, including laparoscopy (2 patients) and thoracoscopy (2 patients), were performed at initial assessment or when clinically indicated. The mean follow-up was 3 years (range, 1 to 8 years). Clinical Features The clinical features, laboratory values, and imaging findings at time of presentation are listed in Table 1. Of 11 patients, 5 patients presented with right upper Figure 2. CD334-positive tumor cells are seen within sinusoids. (Immunostain using antibody to CD34, counterstained with hematoxylin; original magnification 250).
3 528 Ben Haim et al Table 1. Clinical Features, Laboratory Values, and Imaging Findings at Time of Presentation Patient No. Age (yr)/ Sex Symptoms TB (mg/dl) Laboratory Values AP (IU/L) GGTP (IU/L) AST (IU/L) Imaging Liver ALT (IU/L) No. Side Size (cm)* Lung Bone Spleen Other 1 40/M RUQ pain N 123 N 110 N M R /F RUQ pain N 168 N N M R /F RUQ pain N N N N N M B /M RUQ pain N N N N N M B 2? 5 34/M Ascites, jaundice M B D? RPLN (venoocclusive disease) 6 61/M Ascites, jaundice (venoocclusive disease) N M B /M Ascites, jaundice (alcoholic cirrhosis?) M B 20 RLL 8 70/F Atypical chest pain N N N N N M B /F Asymptomatic N N N S R /M Asymptomatic N N N M B /M RUQ pain N N N M B 6 Abbreviations: RUQ, right upper quadrant; TB, total bilirubin; AP, alkaline phosphatase; GGTP, gamma glutamyl transpeptidase; AST, aspartate aminotransferase; ALT, alanine aminotransferase; N, normal; M, multiple; S, single; R, right; B, bilateral; D, diffuse; RLL, right lower lobe; RPLN, retroperitoneal lymph nodes. *Size of largest lesion. Recent referral. In retrospective investigation, asymptomatic but with laboratory and imaging evidence of liver disease 7 years before the referral. When referred, rapid development of jaundice and ascites (see text). Results For evaluation of the results, we divided the patients into three groups: primary resection (2 patients), OLT (5 patients), and observation (5 patients). One patient, first treated with resection and then with OLT, was included in both of those two groups. Patient survival, recurrence or progression of measurable disease, and related symptoms are listed in Table 2. There was no perioperative mortality in the two treatment groups. In the resection group, we found early, rapid, and aggressive recurrence. Although the preoperative and intraoperative assessment suggested localized lobar disease, follow-up CT scans performed 3 months after resection showed multiple lesions in the residual liver (Fig. 3). In the OLT group, there were three recurrences. Two patients died within the first year after OLT, with evidence of massive tumor recurrence in the grafted liver. In another patient in whom intraperitoneal chemotherapy was administered for peritoneal seeding, tumor recurrence in the grafted liver was detected after 4 years, resection was performed, and the patient is alive and free of disease 8 years posttransplantation. Two transplantations were performed in patients with liver failure and severe ascites secondary to Budd- Chiari syndrome/veno-occlusive disease, in the face of extrahepatic involvement. One of these patients is now free of symptoms, with no progression of his extrahepatic lesions, at 2 years posttransplantation. The fifth transplant recipient is alive and disease free at 10 months posttransplantation. Among the 5 patients in the observation group, there was one death. This patient was referred with advanced disease (largest lesion size, 20 cm), liver failure, coexistent alcoholic cirrhosis, and lung metastases. The other 4 patients are alive, with minimal symptoms and stable or minimal progression of their disease on imaging. Four patients are listed for OLT; 3 of these 4 are stable, and their clinical status does not indicate urgent transplantation.
4 Hepatic Epithelioid Hemangioendothelioma 529 Table 2. Treatment and Outcome Patient No. Extrahepatic Disease Treatment Outcome Follow-Up 1 1. R extended lobectomy* 2. OLT 2 Peritoneum Omentum Diaphragm 3 Peritoneum Diaphragm 1. R extended lobectomy Omentectomy Excision of diaphragm Intraperitoneal 5-FU 1. Diagnostic laparoscopy 2. OLT Excision of peritoneal lesions Intraperitoneal 5-FU 3. R hepatectomy 1. Recurrence after resection 2. Recurrence in graft; recurrence-related death Recurrence in liver Alive, symptomatic Liver recurrence 4 years after OLT Currently alive, free of measurable disease 4 1. Diagnostic laparoscopy 2. OLT* Alive, free of measurable disease. 5 Spleen; 1. OLT Alive with stable residual disease, asymptomatic RPLN 6 1. OLT Recurrence in graft and bones; recurrence-related death 7 Lung 1. Open liver biopsy* Disease-related death Spleen 2. Diagnostic thoracoscopy Lung biopsy 2 years Death, 9 mon after OLT 22 mon 8 years 18 mon before OLT 12 mon since OLT 32 mon 7 years 11 mon 8 Bone Alive with stable disease; asymptomatic 12 mon 9 Alive with stable disease; asymptomatic 18 mon 10 Bone Alive with stable disease; asymptomatic 4 years 11 Alive with slow progression; asymptomatic 5 mon Abbreviations: R, right; OLT, orthotopic liver transplantation; 5-FU, 5-fluorouracil; RPLN, retroperitoneal lymph nodes. *Procedures were performed in other institutions. The patients are listed for OLT. Death 6 months after OLT. In retrospective investigation, laboratory and imaging evidence of liver disease 7 years before referral. 1 year of follow-up in our institution. Discussion HEHE is a rare and relatively newly defined entity. The true incidence is unknown, and many of the published cases were initially misdiagnosed. 1,4 The natural course and the prognosis are unpredictable, and there is no correlation between the morphological grading or clinical staging and outcome. 1,4 Some patients are asymptomatic and only incidentally diagnosed, whereas others present with severe liver-related complications. There are reports of prolonged survival without treatment, different degrees of success with a variety of medical modalities or surgical resection, 3 and recently, promising results with OLT. 12 The literature is composed of small and heterogeneous series. Lauffer et al 3 reviewed 127 published cases and tried to evaluate the outcome; however, many of these cases consisted of the same patients, presented repetitively in different publications. The lack of designed comparative studies and the inability to predict the course and outcome for a given patient mandate a very careful interpretation of the results. Lauffer et al 3 proposed radical liver resection as the treatment of choice in the absence of multifocal disease, but only 4 patients with indeterminable outcome are presented. Our impression is that the liver involvement is nearly always multifocal, even when imaging studies show a dominant unilobar lesion, and our experience with local resection is disappointing. Because liver regeneration is dependent on angiogenesis, one possible explanation for the aggressive behavior after resection may be tumor sensitivity to the hepatotrophic growth factors that promote hepatic
5 530 Ben Haim et al Figure 3. Early and aggressive recurrence after resection of apparently localized lesion. Repeated CT scans (A) before, (B) at 3 months, and (C) at 5 months after right hepatic lobectomy. regeneration. The relative richness of specific antigens within the tumor cells may support this theory, but further study is needed to confirm it. Although clinical experience with resection of these tumors is limited, based on our experience, we would hesitate to perform resection for apparently resectable cases of HEHE. Since OLT was accepted as treatment for primary liver tumors, its application in patients with HEHE gained attention, support, and criticism. Madariaga et al reported 71.3% actuarial patient survival and 60.2% actuarial disease-free survival at 5 years post-olt in 16 patients. 12 Interestingly, in their earlier series, there was no correlation between pre-olt spread and post-olt recurrence and survival. 5,11 As in 1 of our patients, they described prolonged disease-free survival after OLT in patients with disseminated disease at presentation. Conversely, patients who had disease confined to the liver developed rapid recurrence and metastases after OLT. Based on the available data, it is impossible to compare OLT results with untreated or medically treated patients. The role of elimination of the primary tumor and the impact of immune suppression on the tumor behavior in patients with extrahepatic disease are not clear. Wood, 15 in the face of a shortage of donor livers, criticized OLT as treatment in these cases. Our impression is that significant symptomatic improvement with relatively stable extrahepatic residual disease can be achieved with OLT. 16 Because life expectancy in this situation is potentially long, extrahepatic disease should not serve as an absolute contraindication. Data-based criteria for patient selection and ideal timing of OLT are not available. In this reality, decision making should be tailored for each case, and the individual rate of progression, severity of symptoms, and degree of response to other modalities of treatment may be important determinants. References 1. Weiss SW, Enzinger FM. Epithelioid hemangioendothelioma: A vascular tumor often mistaken for a carcinoma. Cancer 1982;50: Dail DH, Liebow AA. Intravascular bronchioalveolar tumor [abstract]. Am J Pathol 1975;78:A6.
6 Hepatic Epithelioid Hemangioendothelioma Lauffer JM, Zimmermann A, Krahenbuhl L, Bear HU. Epithelioid hemangioendothelioma of the liver. A rare hepatic tumor. Cancer 1996;78: Ishak KG, Sesterhenn IA, Goodman MZD, Rabin L, Stromeyer FW. Epithelioid hemangioendothelioma of the liver: A clinicopathologic and follow-up study of 32 cases. Hum Pathol 1984;15: Kelleher MB, Iwatsuki S, Sheahan DG. Epithelioid hemangioendothelioma of the liver. Clinicopathological correlation of 10 cases treated by orthotopic liver transplantation. Am J Surg Pathol 1989;13: Miller WG, Dodd GD, Federle MP, Baron RL. Epithelioid hemangioendothelioma of the liver: Imaging findings with pathologic correlation. AJR Am J Roentgenol 1992; 159: Scoazec JY, Lamy P, Degott C, Reynes M, Feldmann G, Bismuth H, et al. Epithelioid hemangioendothelioma of the liver. Diagnostic features and role of liver transplantation. Gastroenterology 1988;94: Demetris AJ, Minervini M, Raikow RB, Lee RG. Hepatic epithelioid hemangioendothelioma: Biological questions based on pattern of recurrence in an allograft and tumor immunophenotype. Am J Surg Pathol 1997;21: Idilman R, Docmeki A, Beyler AR, Bastemir M, Oremci N, Aras N, et al. Successful medical treatment of epithelioid hemangioendothelioma of liver. Oncology 1997;5: Holley MP, Cuschieri A. Epithelioid hemangioendothelioma of the liver: Objective response to hepatic intraarterial 5-FU. Eur J Surg Oncol 1989;15: Marino IR, Todo S, Tzakis AG, Klintmalm G, Kelleher M, Iwatsuki S, et al. Treatment of hepatic epithelioid hemangioendothelioma with liver transplantation. Cancer 1988; 62: Madariaga JR, Marino IR, Karavias DD, Nalesnik MA, Doyle HR, Iwatsuki S, et al. Long-term results after liver transplantation for primary hepatic hemangioendothelioma. Ann Surg Oncol 1995;2: Pichlmayer R, Weimann A, Ringe B. Indications for liver transplantation in hepatobiliary malignancy. Hepatology 1994;20:33S-40S. 14. Van-de-stadt MB, Gelin M, Adler M, Lambilliotte JP. Epithelioid hemangioendothelioma and liver transplantation. Gastroenterology 1989;96: Wood RP. Hepatic epithelioid endotheliomas. Ann Surg Oncol 1995;2: Walsh MM, Hytiroglou P, Thung SN, Fiel MI, Siegel D, Emre S, et al. Epithelioid hemangioendothelioma of the liver mimicking Budd-Chiari syndrome. Arch Pathol Lab Med 1998;122:84-88.
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