Case Report Open Access
Copyright ©The Author(s) 2017. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Hepatol. Dec 28, 2017; 9(36): 1361-1366
Published online Dec 28, 2017. doi: 10.4254/wjh.v9.i36.1361
De-novo hepatocellular carcinoma after pediatric living donor liver transplantation
Samuel Torres-Landa, Department of Gastrointestinal Surgery, Hospital of the University of Pennsylvania, Philadelphia, PA 19104, United States
Armando Salim Muñoz-Abraham, Sukru H Emre, Manuel I Rodriguez-Davalos, Department of Surgery, Yale University School of Medicine, New Haven, CT 06510, United States
Brett E Fortune, Division of Gastroenterology and Hepatology, Weill Cornell Medicine, New York, NY 10021, United States
Ananta Gurung, Department of Pathology, Royal Columbian Hospital, New Westminster, British Columbia V3L 3W7, Canada
Jeffrey Pollak, Department of Radiology and Biomedical Imaging, Yale University School of Medicine, New Haven, CT 06510, United States
Michael L Schilsky, Division of Digestive Diseases and Transplant and Immunology, Department of Medicine and Surgery, Yale University School of Medicine, New Haven, CT 06510, United States
ORCID number: Samuel Torres-Landa (0000-0003-1230-1137); Salim A Muñoz-Abraham (0000-0002-1168-6867); Brett E Fortune (0000-0002-0646-467X); Ananta Gurung (0000-0002-4260-1133); Jeffrey Pollak (0000-0003-0447-0109); Sukru H Emre (0000-0001-7562-8570); Manuel I Rodriguez-Davalos (0000-0002-5070-2719); Michael L Schilsky (0000-0001-9043-0554).
Author contributions: Torres-Landa S, Munoz-Abraham AS, Fortune BE, Emre SH, Rodriguez-Davalos MI, and Schilsky ML contributed with the case report design, collecting the data and writing the manuscript; Gurung A helped with the pathology reports, pathology images description and analysis of the data; Pollak J helped with the radiology reports and analysis of the data.
Informed consent statement: The authors should be aware that at the time of publication, the covered entity does not have actual knowledge (any identifiers described by HIPAA) that the information could be used alone or in combination with other information to identify an individual who is subject of the information. According to the IRB review and HIPAA compliance we have removed all HIPAA identifiers as the consent was unable to obtain.
Conflict-of-interest statement: All the authors have no conflicts of interest to declare.
Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Correspondence to: Manuel I Rodriguez-Davalos, Associate Professor, Department of Surgery, Yale University School of Medicine, 333 Cedar St, New Haven, CT 06510, United States. rodriguezmi@me.com
Telephone: +1-203-7856501 Fax: +1-203-7374033
Received: August 25, 2017
Peer-review started: August 25, 2017
First decision: November 1, 2017
Revised: November 22, 2017
Accepted: December 7, 2017
Article in press: December 8, 2017
Published online: December 28, 2017

Abstract

De-novo malignancies carry an incidence ranging between 3%-26% after transplant and account for the second highest cause of post-transplant mortality behind cardiovascular disease. While the majority of de-novo malignancies after transplant usually consist of skin cancers, there has been an increasing rate of solid tumor cancers over the last 15 years. Although, recurrence of hepatocellular carcinoma (HCC) is well understood among patients transplanted for HCC, there are increasing reports of de-novo HCC in those transplanted for a non-HCC indication. The proposed pathophysiology for these cases has been mainly connected to the presence of advanced graft fibrosis or cirrhosis and always associated with the presence of hepatitis B or C virus. We report the first known case of de-novo HCC in a recipient, 14 years after a pediatric living related donor liver transplantation for end-stage liver disease due to biliary atresia without the presence of hepatitis B or C virus before and after transplant. We present this case report to increase the awareness of this phenomenon and address on the utility for screening and surveillance of hepatocellular carcinoma among these individuals. One recommendation is to use similar guidelines for screening, diagnosis, and treatment for HCC as those used for primary HCC in the pre-transplant patient, focusing on those recipients who have advanced fibrosis in the allograft, regardless of etiology.

Key Words: Liver transplantation, De-novo hepatocellular carcinoma, Living donor liver transplantation, Biliary atresia

Core tip:De-novo hepatocellular carcinoma (HCC) is a rare event compared to other de-novo malignancies, although the number of reported cases are increasing. The pathophysiology has been related with advanced graft fibrosis, cirrhosis and hepatitis viral serology. We report the first case of De-novo HCC 14 years after living related donor liver transplantation for end-stage liver disease due to biliary atresia without positive hepatitis B or C viral serology. Current screening and treatment guidelines have not been well established. This increasing phenomenon challenges us to define the utility of screening and surveillance for hepatocellular carcinoma in these individuals.



INTRODUCTION

Hepatocellular carcinoma (HCC), the most common primary malignancy of the liver, is one of the most lethal and prevalent cancers worldwide. However, the use of liver transplantation (LT) is a well proven treatment approach for patients with low stage tumor. The pathogenesis of HCC typically involves chronic liver injury with regeneration, fibrosis and cirrhosis leading to dysplasia within regenerating nodules with an end result of malignancy[1]. HCC development in a liver allograft occurs most often in the setting of prior HCC where it is defined as recurrence[2]. De-novo tumor formation that arises in the transplanted graft without evidence of tumor in the previously explanted liver is uncommon and is mainly seen in patients with advanced graft fibrosis or cirrhosis and associated with the presence of hepatitis B or C viral infection[3]. The literature reveals only 15 documented cases of de-novo HCC after LT[4-15]. We report the first case of de-novo HCC occurring 14 years after a pediatric patient received a living related donor LT for end stage liver disease secondary to biliary atresia.

CASE REPORT

A 29-year-old male with a history of biliary atresia with failed Kasai procedure complicated with progressive cirrhosis and portal hypertension that received a left lateral segment living donor liver transplant (LDLT) from his biological father at 15 years of age. His immunosuppressive regimen included tacrolimus, and sirolimus. Eleven years after his LDLT, he developed advanced liver fibrosis and portal hypertension that manifested as refractory ascites. He received a splenectomy and a central spleno-renal shunt that eventually failed. He then underwent a side-to-side porto-caval shunt (PCS) at age 27 years. After 2 years with controlled disease, he presented with recurrent ascites and overt hepatic encephalopathy (HE) related to his progressive graft failure. His clinical course was also complicated by severe protein losing enteropathy due to his worsening portal hypertension (sprue was excluded by small bowel biopsy). Other causes of hypoalbuminemia were ruled out (e.g., kidney injury secondary sirolimus, as evidenced by 24-h urine collection with minimal protein and normal creatinine). Liver biopsy at this time showed stage 3-4 fibrosis. In addition, there was a paucity of interlobular bile ducts with degenerative changes in the remaining ducts, features compatible with chronic allograft rejection. A few months after, an abdominal ultrasound of the graft revealed a hepatic mass measuring 2.9 cm × 2.2 cm located in segment 2/3 and no evidence of intrahepatic duct dilation. Dynamic CT imaging showed a 3 cm lesion in the left lateral segment that was slightly hypodense and indeterminate in nature (Figure 1). A dynamic magnetic resonance imaging (MRI) using liver mass protocol was performed due to the indeterminate nature of the lesion on CT and demonstrated increased vascularity of the lesion, raising suspicion for HCC. An ultrasound-guided percutaneous biopsy of the mass revealed a well-differentiated HCC (Figure 2). Chest CT scan and bone scan demonstrated no evidence of extra hepatic disease. Alpha-fetoprotein (AFP) level was slightly elevated at 17 ng/mL (normal < 6 ng/mL). Anti-HBcAb (anti-hepatitis B core total antibodies) at this time and a year before showed negative results. The lesion was subsequently treated by percutaneous microwave ablation (PMWA).

Figure 1
Figure 1 Dynamic computerized tomography scan imaging showing indeterminate 3 cm lesion in the left lateral segment.
Figure 2
Figure 2 Ultrasound-guided liver biopsy. A: Biopsy of the mass shows a solid growth pattern of hepatocytes (H+E, 100 ×); B: Neoplastic hepatocytes contain hyperchromatic, pleomorphic and enlarged nuclei (H+E, 200 ×); C: Reticulin stain demonstrates thickened trabeculae and decreased staining in the lesion (200 ×).

Follow up MRI was performed 1.5 mo after the ablation and showed no residual tumor (Figure 3). The patient was subsequently listed for repeat liver transplantation. However, while on the wait-list he developed a second post-transplant malignancy, an EBV negative Burkitt’s type lymphoma. He received chemotherapy for the lymphoma but succumbed to complications due to the treatment that was in part limited by his advanced liver disease.

Figure 3
Figure 3 Follow-up magnetic resonance imaging showing the ablation cavity in segment III measuring 2. 8 cm × 2.5 cm without evidence of residual tumor.
DISCUSSION

Liver transplantation provides the highest survival rates among patients with decompensated cirrhosis and complications of portal hypertension but recipients have a 2-4 fold increased risk of developing de-novo malignancies when compared to matched healthy controls[16]. De-novo malignancies represent 30% of post-transplant deaths and one of the most common causes of death in patients that survive beyond a year after transplantation[3,17]. Although there is an increased risk of developing malignancies, De-novo HCC is uncommon[3,17].

When HCC after transplantation is identified, it is crucial to know if it is a recurrent malignancy as this carries a poor prognosis. Travesani et al[17] have proposed an algorithm where they suggest suspicion primary features of a recurrent case including lymph node invasion, macro and microvascular invasion, tumor size > 5 cm, high grade tumor, bi-lobar involvement and high alpha fetoprotein levels. Secondary features include early occurrence, < 2 years, and extra hepatic localization. Without the presence of these characteristics, the suspicion turns towards a de-novo HCC. Other common clinical factors that suggest a de-novo case, even in patients transplanted for or with a previous HCC, are older donor age, alcoholic liver disease, viral hepatitis, recurrent liver disease and exposure to environmental carcinogens. Although the clinical features cannot guarantee the distinction with certainty, molecular techniques may permit differentiation of donor from recipient origin[17]. In addition, allografts have a certain degree of hepatocyte chimerism (graft and recipient cells) that also correlates with the degree of hepatic injury and is strongly associated with hepatitis[18].

The pathogenesis of HCC appears to be related to chronic hepatic inflammation that eventually leads to fibrosis and cirrhosis. The inflammatory microenvironment in the liver leads to a proliferative state that can promote dysplasia and eventually malignancy regardless of the underlying liver disease[1]. Graft rejection, which is an immunological surge against detected antigens found within the graft, can generate a chronic inflammatory state[19] and create an environment that promotes oncogenesis and dysplasia. Other well-established risk factors for promoting carcinogenesis include the use of immunosuppressive therapy as it reduces immune surveillance, increased age and gender specific cancer risks, development of insulin resistance and exposure to viral infections (HBV and HCV)[3,16,17].

From the 16 cases of de-novo HCC occurrence reported so far in the literature, 14 had positive viral serology (HVB or HCV) (Table 1). In these cases the viral infection likely drove tumorogenesis. However, this is a novel case describing a de-novo HCC after a LDLT in a pediatric patient. Our case represents the development of a hepatic tumor in the setting of advanced hepatic fibrosis, likely from chronic allograft rejection, without any underlying viral disease or other chronic infection. Interestingly both biliary atresia itself and Kasai procedure have been associated with the development of HCC[20-22]. However, given the 14 year gap from transplant to development of HCC, this probably did not contribute to the development of HCC in this particular patient.

Table 1 Modified from Saab et al[14].
PatientRef.OLT indicationAgeGenderImmunosuppressionInterval (yr)Type of donorPVSApproach after de-novo HCC
1Saxena et al[4]HCV and ALD63MCYA, AZA and Pred7DDYesRetransplant
2Levitsky et al[5]HCV and ALD48MCYA, AZA and Pred5N/AYesNR
3Croitoru et al[6]HCV and NAFLD61MCYA and Pred6DDYesRetransplant
4Flemming et al[7]HBVNRMNR9DDYesHepatic Resection
5Flemming et al[7]HBVNRMNR8DDYesRetransplant and Hepatic Resection
6Torbenson et al[8]HBV51MNR8.5DDYesRetransplant
7Kita et al[9]HBV43MNR14NAYesRetransplant
8Yu et al[10]HBV36MTAC, MMF andPred2LDYesRFA
9Sotiropoulos et al[11]Budd-Chiari Syndrome61FNR22NAYesTACE
10Sotiropoulos et al[11]ALD65MNR5NANRRFA
11Vernadakis et al[12]ALD59MCYA, MMF and Pred3DDNoHepatic Resection
12Tamè et al[13]HCV54MTAC and Pred6DDYesTACE
13Saab et al[14]HCV47FTAC and MMF19-YesTACE, RFA, Sorafenib, Retransplant
14Tamè et al[13]SSC44MTAC and Pred6DDYesSorafenib
15Navarro Burgos et al[15]HCV and HBV45MNR0.75DDYesTACE
16The present caseBiliary atresia29MTAC and Sirolimus14LDNoPMWA

Although current treatment guidelines for De-novo HCC after LT have not been well established, it was suggested that these cases be approached according to the current guidelines for primary and recurrent HCC[17]. The strategies that have been used in the reported cases to date are: re-transplantation (n = 6)[4,6-9,14], trans-arterial chemoembolization (TACE) (n = 4)[11,13-15], hepatic resection (n = 3)[7,12], radiofrequecy ablation (RFA) (n = 3)[10,11,14], medical therapy with Sorafenib (n = 2)[13,14] and PMWA in our case. Two of the reported cases used more than one procedure[7,14].

Proper age and gender appropriate cancer screening and surveillance is universally practiced among transplant recipients to diagnosis early stage malignancy. Since approximately one-fifth of all post-transplant deaths are related to de-novo neoplasms (including de-novo HCC)[3] and the incidence of HCC recurrence can be as high as 18.3% after transplant[2], many transplant programs have in place post-LT screening and surveillance for HCC in patients transplanted for HCC along with other appropriate cancer screening and surveillance[3]. However, these protocols for post-LT screening and surveillance are not uniform amongst centers as there is a general lack of evidence base for deciding on a specific protocol. This remains to be established.

In summary, we describe the first case of de-novo HCC after living donor liver transplantation in a patient with a prior history of biliary atresia who developed graft dysfunction and complications of portal hypertension. This case and the increase in reports of de-novo development of HCC in liver grafts of patients without HCC prior to LT challenges us to define the incidence of development of HCC in post-LT patients with chronic injury and graft fibrosis to determine when there is utility in recommending screening and surveillance of these individuals for HCC, and design appropriate protocols to carry this out.

ARTICLE HIGHLIGHTS
Case characteristics

A 29-year-old male with a history of biliary atresia with failed Kasai procedure complicated with progressive cirrhosis and portal hypertension that received a left lateral segment living donor liver transplant (LDLT) from his biological father at 15 years of age.

Clinical diagnosis

Biliary atresia, complicated with progressive cirrhosis and portal hypertension that received a left lateral segment living donor liver transplant LDLT.

Differential diagnosis

A case of de-novo hepatocellular carcinoma (HCC) (confirmed by ultrasound-guided percutaneous biopsy of the mass) 14 years after a pediatric living related donor liver transplantation for end-stage liver disease without positive hepatitis B or C viral serology.

Imaging diagnosis

Follow up magnetic resonance imaging was performed 1.5 mo after the ablation and showed no residual tumor.

Treatment

The lesion was subsequently treated by percutaneous microwave ablation. The patient was subsequently listed for repeat liver transplantation. Current screening and treatment guidelines have not been well established.

Experiences and lessons

This increasing phenomenon challenges us to define the utility of screening and surveillance for HCC in these individuals.

Footnotes

Manuscript source: Unsolicited manuscript

Specialty type: Gastroenterology and hepatology

Country of origin: United States

Peer-review report classification

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Grade D (Fair): D

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P- Reviewer: Chok KSH, Coelho JCU S- Editor: Kong JX L- Editor: A E- Editor: Wang CH

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