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1 CLINICAL GASTROENTEROLOGY AND HEPATOLOGY 2009;7: Liver Transplantation in Patients With Nonalcoholic Steatohepatitis-Related Hepatocellular Carcinoma SHAHID M. MALIK,* PARIJAT A. GUPTE,* MICHAEL E. DE VERA, and JAWAD AHMAD* *Division of Gastroenterology, Hepatology and Nutrition and Thomas E. Starzl Transplantation Institute, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania See related article, Marrero JA et al, on page 110 in Gastroenterology. BACKGROUND & AIMS: The increasing incidence of hepatocellular carcinoma in the United States is only partially accounted for by hepatitis C virus (HCV) infections. The prevalence of hepatocellular carcinoma in patients with nonalcoholic steatohepatitis (NASH) is not known; guidelines from the American Association for the Study of Liver Diseases do not recommend surveillance imaging. We sought to determine the prevalence of hepatocellular carcinoma among patients undergoing liver transplantation for NASH-related cirrhosis and their outcome after surgery, compared with controls. METHODS: We reviewed the records of adult patients with NASH cirrhosis who underwent liver transplantation by using a prospectively collected database from a single center. Data from patients with NASH cirrhosis were compared with matched controls who received transplantation for primary biliary cirrhosis/primary sclerosing cholangitis, alcoholic liver disease, or HCV. RESULTS: Seventeen of 98 patients (17%) with NASH cirrhosis were diagnosed with hepatocellular carcinoma. The mean age was 63 years, and 70% were male. Six patients were diagnosed with hepatocellular carcinoma incidentally on explant. Survival after liver transplantation was 88% after mean follow-up of 2.5 years. The number of NASH patients known to have hepatocellular carcinoma before liver transplantation was greater than the number of patients with primary biliary cirrhosis/primary sclerosing cholangitis and comparable to the number of patients with alcoholic liver disease and HCV. CONCLUSIONS: Patients with NASH cirrhosis are at risk for developing hepatocellular carcinoma; patients with NASH cirrhosis, especially men older than 50 years, should undergo surveillance imaging. Patients with NASH and hepatocellular carcinoma have good outcomes after liver transplantation. To view this article s video abstract, go to the AGA s YouTube Channel. There are approximately 1 million new cases of primary hepatocellular carcinoma (HCC) diagnosed annually worldwide. Liver cancer is the sixth most common cancer and the third most common cause of death from cancer. The majority of cases of HCC develop in patients with chronic liver disease or cirrhosis. The major risk factor for the development of HCC worldwide is infection with hepatitis B virus (HBV). 1 HCC complicating cirrhosis has a high mortality rate, unless it is detected in its early stages. Most cases do not survive a year. 2 HCC is now a leading cause of death in patients with cirrhosis. 3 5 The incidence of HCC in the United States has doubled during the last 30 years. 6 The cause of this increase is incompletely understood. The increasing incidence in the United States has been partially attributed to hepatitis C virus (HCV)- associated cirrhosis, with HBV and alcoholic liver disease (ALD) playing a smaller role. 7 Up to one half of HCC cases in the United States, however, are idiopathic, suggesting that other risk factors are responsible for this increase. 8 Recent studies have suggested that the epidemic rise in obesity and diabetes mellitus (DM) could account for at least a portion of these idiopathic cases Although it is unproved, some experts hypothesize that the relationship of obesity and DM to HCC is mediated through the development of nonalcoholic steatohepatitis (NASH). 11 As the incidence of obesity, DM, and other features of metabolic syndrome increases, so too does the incidence of NASH. It is estimated that nearly 10 million Americans have NASH, making it the most common cause of chronic liver disease in the United States. 12 NASH cirrhosis is likely to become a leading indication for liver transplantation (LT) in the near future. 13 Although NASH is known to progress to end-stage liver disease, little is known about the incidence of HCC in patients with NASH cirrhosis. There is growing evidence, however, indicating that HCC should be considered in the natural history of progressive NASH. The first reported case of NASH-related HCC was published in Since then, several case reports and case series have documented the occurrence of HCC in patients with NASH The American Association for the Study of Liver Disease (AASLD) currently recommends screening and surveillance for HCC in high-risk groups, including hepatitis B carriers and Abbreviations used in this paper: AASLD, American Association for the Study of Liver Diseases; AFP, alpha-fetoprotein; ALD, alcoholic liver disease; BMI, body mass index; CIT, cold ischemic time; CTP, Child- Turcotte-Pugh; CT, computed tomography; DM, diabetes mellitus; FAL, fractional allelic loss; HBV, hepatitis B virus; HCC, hepatocellular carcinoma; HCV, hepatitis C virus; HTN, hypertension; LOH, loss of heterozygosity; LOS, length of stay; LT, liver transplantation; MELD, Model for End-Stage Liver Disease; MRI, magnetic resonance imaging; NASH, nonalcoholic steatohepatitis; PBC, primary biliary cirrhosis; PSC, primary sclerosing cholangitis; US, ultrasound; WIT, warm ischemic time by the AGA Institute /09/$36.00 doi: /j.cgh
2 July 2009 LIVER TRANSPLANT FOR NASH HCC 801 cirrhosis caused by hepatitis C, alcohol, hemochromatosis, and primary biliary cirrhosis (PBC). Although the guidelines acknowledge that cirrhosis from other diseases (NASH, alpha 1 - antitrypsin deficiency, and autoimmune hepatitis) puts patients at an increased risk for the development of HCC, they state that in these patients no recommendations for or against surveillance can be made because of a lack of data (that) precludes an assessment of whether surveillance would be beneficial. 21 The aims of this study were 2-fold: (1) to determine the incidence of HCC in patients who underwent LT for a diagnosis of NASH cirrhosis compared with the other most common indications for LT in the United States and (2) to determine the outcome of patients with HCC and NASH cirrhosis undergoing LT. Materials and Methods We retrospectively reviewed the records of all adult patients undergoing LT for a diagnosis of NASH cirrhosis by using a prospectively collected database at a single center. Patients were considered to have a diagnosis of NASH cirrhosis on the basis of histopathologic findings and if they fulfilled the following criteria: absence of alcohol history, exclusion of other forms of chronic liver disease, on the basis of history, laboratory testing, histology, and absence of potential exposures to hepatotoxins or medications associated with hepatic steatosis. All patients underwent extensive serologic testing, including testing for hepatitis B (hepatitis B surface antibody, surface antigen, and core antibody), hepatitis C (hepatitis C second-generation enzyme-linked immunosorbent assay, HCV RNA), hemochromatosis (serum iron, % saturation, total iron binding capacity, ferritin, and HFE genetic testing if indicated), Wilson disease (ceruloplasmin levels), alpha 1 -antitrypsin deficiency (alpha 1 -antitrypsin levels and phenotype), autoimmune hepatitis (antinuclear antibody titers, anti smooth muscle antibody titers, anti liver kidney microsomal antibody titers, and quantitative immunoglobulin levels), and PBC (antimitochondrial antibody titers). All pre-lt imaging (ultrasound [US] and either triphasic computed tomography [CT] scan or magnetic resonance imaging [MRI]) reports were reviewed. All explants were examined by experienced hepatopathologists. All explant biopsy reports and available biopsy reports before transplant were reviewed to ensure findings consistent with NASH or NASH cirrhosis. Histologic criteria for NASH included macrovesicular hepatic steatosis, Mallory s hyaline, ballooning degeneration, scattered predominantly neutrophilic inflammation, and pericentral and perisinusoidal fibrosis. 22 Demographic data collected included recipient characteristics (age, sex, race, body mass index [BMI], history of alcohol or illicit drug use, medical history, laboratory data, Model for End-Stage Liver Disease [MELD] score, Child-Turcotte-Pugh [CTP] score, and the number of patients on dialysis or intubated before transplant), patient survival in days, retransplantation, and cause of death. Donor characteristics included age, sex, race, BMI, cause of death, and percent steatosis on biopsy (when available). Surgical cold ischemia times (CITs) and warm ischemia times (WITs), length of operation, and total transfusion requirement during the operation were also noted. Outcome after LT was determined by (1) patient survival, defined as short-term (30 days) and long-term (1, 3, and 5 years), and (2) length of stay (LOS) after transplant, defined as number of hospital days (intensive care unit or otherwise) in patients who were eventually discharged from the hospital to home, rehabilitation, or nursing facility. Incidental HCC was defined as a cancer found only on pathologic evaluation of the explanted native liver, without evidence on pre-lt imaging. Although pretransplant alphafetoprotein (AFP) was reviewed on all patients, elevated levels were not considered diagnostic of HCC before transplant. This is in concordance with previously published data on the definition of incidental HCC. 23,24 Explant reports from all patients with HCC were reviewed. The number of tumors, largest tumor size, tumor differentiation, evidence of microscopic vascular invasion, pathologic TNM classification, pathologic staging, and genetic analysis/ loss of heterozygosity (LOH) were noted. HCC for topographic genotyping was performed on 9 of 17 (52.9%) patients. In these patients, microdissected targets were performed on HCC lesions to determine allelic imbalance or LOH. The fractional allelic loss (FAL) rate was defined as the fraction of mutated markers divided by the total number of informative markers. On the basis of previously published data, an FAL of 0.3 was supportive of indolent behavior, and an FAL 0.3 indicated the capacity for aggressive behavior. 25 Patients with HCC (both known and incidental) are followed at our institution for recurrence with either CT or MRI of the chest, abdomen, and pelvis every 3 months for the first year, every 6 months for the next year, and then annually. Comparison Groups Patients with NASH cirrhosis were compared in a 1:2 ratio with patients in each of 3 control groups (total 588 patients) who were transplanted for cholestatic liver disease (PBC/primary sclerosing cholangitis [PSC]), ALD, or HCV. The control groups were matched (in order of priority) for age, sex, MELD score, and year of transplant. Patients with NASH-related HCC were also compared with all patients transplanted at our center with a diagnosis of HCC during the last 15 years with etiologies other than NASH. Statistical Analysis Continuous variables were compared by using Student t test. Categorical variables were compared by using 2 test. Survival after LT was calculated by using the Kaplan Meier method and compared by using the log-rank test. Data are expressed as means. All analyses were performed by using Stata 8.0 (Statacorp, College Station, TX). The study was approved by the University of Pittsburgh Institutional Review Board. Results Of 2012 adult patients who underwent LT at our center from July 6, 1997 to June 31, 2008, we identified 143 patients with a diagnosis of NASH cirrhosis. After review, 45 patients were eliminated for the following reasons: cryptogenic cirrhosis (n 12), evidence of alpha 1 -antitrypsin deficiency (n 7), autoimmune hepatitis (n 5), alcohol use (n 5), hemochromatosis (n 4), HCV (n 3), HCV/ALD (n 2), Wilson disease (n 2), methotrexate-induced liver injury (n 2), possible acetaminophen toxicity (n 1), fulminant hepatic failure (n 1), and HBV/ALD (n 1), leaving 98 patients (4.8%
3 802 MALIK ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 7, No. 7 Table 2. Donor, Surgical, and Mortality Data of 81 Patients With NASH Cirrhosis Undergoing LT Compared With 17 With NASH-Related HCC NASH (n 81) NASH HCC (n 17) P value Age (y) Sex (male) 42 (51.9%) 11 (64.7%).24 Race (white) 69 (85.2%) 15 (88.2%).55 BMI (kg/m 2 ) Live donor 10 (12.0%) 3 (17.6%).40 CIT (min) WIT (min) Operating room time (min) PRBC transfusions during LT (units) Figure 1. Flow diagram of 2012 adult LT recipients showing criteria used for diagnosis of NASH cirrhosis. of 2021 total adult LTs) transplanted with a primary diagnosis of NASH cirrhosis (Figure 1). Most of the 12 patients with cryptogenic cirrhosis had clinical features consistent with NASH, but a diagnosis of NASH could not be confirmed by histology (likely burnt out NASH ). We elected not to include these 12 patients among our NASH cohort. Seventy-one of 98 patients had pretransplant biopsies consistent with a diagnosis of NASH. The remaining 27 patients included in the cohort had explant biopsy findings diagnostic for NASH. Of the 71 patients who had pre-lt biopsies diagnosing NASH, 49 had explant findings consistent with NASH, Table 1. Baseline Recipient Characteristics and Mortality Data of 81 Patients With NASH Cirrhosis Undergoing LT Compared With 17 Patients With NASH Cirrhosis and HCC NASH (n 81) NASH HCC (n 17) P value Age (y) Range Median Sex (male) 32 (39.5%) 12 (70.6%).02 Race (white) 79 (97.5%) 16 (94.1%).44 BMI (kg/m 2 ) BMI 30 (kg/m 2 ) 49 (60.5%) 12 (70.6%).31 DM 59 (72.8%) 12 (70.6%).53 HTN 41 (50.6%) 8 (47.1%).50 DM HTN 36 (44.4%) 6 (35.3%).34 Metabolic syndrome 49 (60.5%) 12 (70.6%).31 CTP score Calculated MELD score Intubated 6 (7.4%) 0.31 Dialysis 8 (9.9%) 3 (17.6).29 Intubated dialysis 3 (3.7%) Day mortality 8 (9.9%) 2 (11.1%).55 1-Year mortality 16 (19.8%) 2 (11.1%).35 3-Year mortality 23 (28.4%) 2 (11.1%).13 5-Year mortality 25 (30.9%) 2 (11.1%).09 LOS (days) PRBC, packed red blood cells. and 22 (31%) had developed significant fibrosis or complete cirrhosis with little remaining diagnostic features of NASH (Figure 1). Baseline characteristics of all patients and donors (98 NASH and 588 controls) and their outcomes after LT have been documented elsewhere. 26 Of the 98 NASH patients, 17 (17.3%) were diagnosed with HCC. The characteristics of recipients and mortality data with HCC and those without HCC are summarized in Table 1. Donor and surgical characteristics are summarized in Table 2. The mean age of patients with HCC was years. Of the 17 patients, 16 were white, and 1 was Asian. The mean BMI was 33.0 kg/m 2. Only 1 patient had a BMI 29 kg/m 2 ; twelve of the 17 patients were obese (BMI 30 kg/m 2 ). Seventy percent of patients carried a diagnosis of DM before transplant, and 47% had hypertension (HTN). Twelve of the 17 patients with HCC and NASH cirrhosis met criteria for metabolic syndrome (with criteria defined by the American Association of Clinical Endocrinologists 27 ). There were significantly more men in the HCC cohort (70.6% versus 39.5%, P.02). Tumor characteristics are outlined in Table 3. Eleven patients were known to have HCC before LT. Six of these patients were treated before LT with chemoembolization. All 17 patients had histologic evidence of cirrhosis. Six patients had HCC discovered incidentally on examination of the explant. All but one of the incidental tumors were less than 2.5 cm (9 tumors, mean size 1.7 cm). One patient with an incidental tumor discovered on explant had an AFP of 882 ng/ml. The explant revealed a 5-cm tumor. Although the preoperative CT scan read the corresponding lesion as an area of fatty infiltration, because of the high suspicion for malignancy, the patient was listed with a MELD upgrade. One patient (case 14) was diagnosed with a mass on pre-lt imaging (with normal AFP and CA19-9) and was being treated with chemoembolization. Explant analysis of the tumor confirmed the presence of a mixed HCC and cholangiocarcinoma. Another patient (case 16) was diagnosed with a 4.5-cm welldifferentiated HCC. The patient was treated with chemoembolization and 4 months after diagnosis underwent LT. Analysis of the explanted liver revealed no evidence of viable tumor. Two patients (cases 4 and 12) would have been considered outside of Milan criteria on the basis of explant findings. Case 4 underwent an MRI before LT that revealed 3 lesions, the
4 July 2009 LIVER TRANSPLANT FOR NASH HCC 803 Table 3. Tumor Characteristics of 17 NASH Patients With HCC Undergoing LT Case Age (y) Sex Race BMI (kg/m 2 ) DM HTN K/I AFP (ng/ml) Diff No. of tumors Largest tumor explant (cm) Microscopic vascular invasion TNM Pathologic stage LOH 1 69 M W N N I 4 Mod N T2NxMx II NP 2 68 M W Y Y K 1151 Mod Y T2NxMx II NP 3 56 M W Y Y I 882 Mod 1 5 Y T2NxMx II NP 4 72 F W Y N K 4 Well N T3N0Mx IIIA 10% 5 64 M W N N K 2 Mod 2 3 Y T3N0Mx IIIA NP 6 65 M W Y N K 137 Well 1 8 N T3N0Mx IIIA NP 7 59 M W N N I 8 Mod N T1N0Mx I 13% 8 57 F W Y N I 4 Well N T2NxMx II NP 9 63 F W N Y I 2 Well N T2NxMx II NP M A Y Y K 5 Mod 1 4 N T1N0Mx I 40% M W Y Y I 2 Mod N T2NxMx II 22% M W Y N K 10 Mod 10 4 Y T2NxMx II 38% M W Y Y K 2 Poor Y T2N0Mx II 77% M W Y Y K 3 Mod N T2N0Mx II 15% M W Y N K 6 Mod N T2NxMx II 47% F W N Y K 13 Well N T1N0Mx I NP F W Y N K 12 Mod 1 4 N T1N0Mx I 19% W, white; A, Asian; N, no; Y, yes; K, known; I, incidental; Diff, tumor differentiation; Mod, moderately differentiated; Well, well-differentiated; Poor, poorly differentiated; NP, not performed. largest of which was 3 cm, and so the patient was within Milan criteria before listing. Case 12 was a patient with biopsy-proven HCC. He underwent a CT scan 3 months before LT that revealed 8 lesions; the largest was 4 cm. The patient was treated with 1 round of chemoembolization before transplant, with significant improvement on the basis of follow-up imaging. Because he was outside Milan criteria, he and his family were counseled and were agreeable to live donor transplantation. There was no difference in 5-year survival between patients transplanted for NASH cirrhosis with and without HCC (Figure 2). Patient survival was 88% at a mean follow-up of 2.5 years (range, 3 months 6.5 years). One death was immediately postoperative and cardiac-related. The other death occurred 6 months after LT and was related to infection. The 15 remaining patients have been followed after LT with serial imaging. One patient (case 13) was noted to have pulmonary nodules on Figure 2. Kaplan Meier survival curve for 81 patients transplanted for NASH cirrhosis versus 17 patients transplanted for NASH HCC. P.14 by log-rank (analysis time in days). imaging 6 months after LT. Biopsy of the nodules showed metastatic HCC. Despite being started on sorafenib, most recent imaging showed brain lesions concerning for metastatic disease. This was the only patient who had poorly differentiated carcinoma on the explant and had the most aggressive biology of all patients who underwent genetic analysis. There was no evidence of recurrent disease on surveillance imaging in the remaining patients. Three of the 17 patients with HCC received live donor transplants. Five of the 11 patients with known HCC were given MELD upgrades, as was the patient with an elevated AFP of 882 ng/ml. Table 4 details the breakdown of known, incidental, and total HCCs between the 4 groups. The total number of primary cancers (known incidental) in the NASH HCC cohort was higher when compared with those with PBC/PSC and comparable to the ALD group. Nearly 28% of patients with HCV had a diagnosis of HCC at the time of LT, which was the highest among the 4 groups. When comparing the 17 patients with HCC and NASH with all patients who underwent transplantation at our institution during the last 15 years with a diagnosis of HCC (n 430: 32% HCV, 23% ALD, 12% HBV, 8% cryptogenic, 7% HCV/ALD, 5% PBC/PSC, 3% autoimmune, 2% hemochromatosis, 1% alpha 1 - antitrypsin deficiency, 3% other), NASH patients with HCC were older and heavier and had a higher incidence of pre-lt DM and HTN (Table 5). There was no difference in the total number of HCCs at the time of LT between these 2 groups. Five-year survival after LT was comparable between the 2 groups (Figure 3). Because a large percentage of cryptogenic cirrhosis is likely to be burnt out NASH, the analysis was also performed by including patients with cryptogenic cirrhosis within the NASH cohort, and outcomes were unchanged. Discussion Because the incidence of HCC in cirrhosis caused by NASH is unknown, it is not possible to assess whether surveil-
5 804 MALIK ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 7, No. 7 Table 4. Number of Known, Incidental, and Total HCCs at the Time of LT for NASH Compared With PBC/PSC, ALD, and HCV Known Incidental Total NASH (n 98) 11 (11.2%) 6 (6.1%) 17 (17.3%) PBC/PSC (n 198), P value 3 (1.5%), (5.6%), (7.1%),.01 ALD (n 198), P value 18 (9.1%),.35 9 (4.5%), (13.6%),.25 HCV (n 198), P value 26 (13.1%), (14.6%), (27.8%),.03 NOTE. P value comparison vs NASH cohort. lance might be effective or cost-efficient. Because of this, the most recent AASLD practice guidelines cannot give recommendations on whether this group should be surveyed for HCC. This study demonstrated that patients with NASH cirrhosis evaluated and then undergoing LT have a 17.3% incidence of HCC, suggesting that surveillance imaging for HCC is required, particularly because one third of the cancers were only discovered in the explanted liver. The incidence of known primary liver cancers in patients with NASH cirrhosis was significantly higher when compared with those with PBC/PSC and comparable to patients with HCV cirrhosis and ALD, all groups in which the current guidelines recommend routine surveillance. Before the present study, fewer than 40 cases of HCC associated with NASH had been reported in the literature (excluding patients with cryptogenic cirrhosis who likely had NASH cirrhosis in retrospect). Interestingly, the majority (89%) of previously described cases were reported in Japan. The 17 patients described here were younger but had a similar sex distribution and similar features of metabolic syndrome. The younger age in our cohort likely reflects a selection bias in the listing of transplant recipients. Despite the multiple medical comorbidities, patients with NASH and HCC had good outcomes after LT. Patient survival at a mean follow-up of approximately 2.5 years was an excellent 88%. These results are very good, considering the 3-year survival rate of small, untreated HCC in patients with cirrhosis is only 25%. 28 Five-year survival after LT was comparable to those Table 5. Recipient Characteristics of 430 Patients Undergoing LT With HCC (Excluding NASH) Compared With 17 Patients With NASH- Related HCC HCC non-nash (n 430) NASH HCC (n 17) P value Age (y) Range Median Sex (male) 339 (78.8%) 12 (70.6%).12 Black 28 (6.5%) 0.01 BMI (kg/m 2 ) BMI 30 (kg/m 2 ) 115 (26.7%) 12 (70.6%).0001 DM 91 (21.2%) 12 (70.6%).0001 HTN 87 (20.2%) 8 (47.1%).01 DM HTN 41 (9.5%) 6 (35.3%).01 AFP (ng/ml) AFP % (26.0%) 3 (17.6%).32 Incidence of total 430/2514 (17.1%) 17/98 (17.3%).52 HCCs Known 160 (6.3%) 11 (11.2%).05 Incidental 270 (10.7%) 6 (6.1%).09 without HCC. Only 1 patient was found to have recurrence of disease. The 2 deaths among the 17 patients were within 1 year of transplant and not related to recurrence of cancer. As evidenced by the current study and previous studies, a significant number of patients with NASH have features of metabolic syndrome. Not surprisingly, patients with NASH cirrhosis were significantly more obese and had a higher incidence of pre-lt DM and HTN, compared with controls and with all non-nash patients with HCC transplanted at our center during the last 15 years. Obesity has been confirmed to lead to an increased risk for HCC in several studies, as has diabetes However, in the current study, although patients with NASH were significantly heavier and had a higher incidence of pre-lt DM and HTN versus the 3 control groups (and versus all patients transplanted with HCC), there was no statistical difference in these 3 variables among NASH patients with and without HCC, perhaps indicating that factors independent of metabolic syndrome might play a role in the neoplastic process. The mechanism of carcinogenesis in patients with NASH is not understood. Studies performed on genetically obese, insulin-resistant ob/ob mice might provide some insight into factors involved in the development of liver cancer in NASH. Lipid peroxidation, free radical oxidative stress, and hepatocyte proliferation in the setting of insulin resistance are hypothesized to contribute to the process of initiating malignant transformation in the setting of what was previously benign steatosis. 34,35 Both increasing age and male sex are known risk factors for HCC in patients with cirrhosis Patients with NASH cirrho- Figure 3. Kaplan Meier survival curve for 430 patients undergoing LT with HCC (non-nash related) versus 17 patients transplanted for NASH HCC. P.15 by log-rank (analysis time in days).
6 July 2009 LIVER TRANSPLANT FOR NASH HCC 805 sis and HCC were on average 5 years older than all other patients transplanted for HCC at our institution. This might indicate either that the onset of NASH occurs later in life, or that decompensation and malignant degeneration occur more slowly in patients with NASH as compared with other forms of chronic liver disease. Although 55% of our NASH cohort was female, only 5 of the 17 patients with HCC were women. This is in concordance with known data that men are far more likely to develop HCC than women. 37,38 The reported incidence of incidental HCC is highly variable, ranging from less than 10% 24 to as high as 60%. 39 In our study the incidence (from a total of 686 patients) was 8.0%. The incidence of incidental carcinoma from all patients with HCC (n 430) at our center during the last 15 years was 11.9%. There were several limitations to the current study. Given the retrospective nature of the study, it was not always possible to determine exactly when patients were diagnosed with NASH cirrhosis and in what time frame they developed HCC. There is a selection bias inherent in listing patients for LT, and so our data do not give a true reflection of the incidence of HCC in patients with NASH, because patients who were very old or obese or who had too large or numerous tumors would not have been listed. Another limitation is the relatively short mean follow-up of 2.5 years in our cohort. However, all recent studies examining recurrent HCC after LT have found that most patients who will experience recurrence will do so within the first year, and nearly all who develop recurrence will declare themselves within the first 3 years after transplant In conclusion, the current study confirms that HCC is part of the natural history of patients with NASH cirrhosis listed and undergoing LT, with the number of known cancers greater than that seen with cholestatic liver disease and comparable to ALD and HCV. The current findings suggest that surveillance imaging for HCC in patients with NASH cirrhosis might be warranted. Age and sex likely play a role in the incidence, and, hence, extra vigilance should be paid to men with NASH cirrhosis older than the age of 50. Furthermore, if detected early, the outcome after LT for patients with NASH and HCC is comparable to other causes of HCC. Supplementary Data Note: To access the supplementary material accompanying this article, visit the online version of Clinical Gastroenterology and Hepatology at and at doi: /j.cgh References 1. Parkin DM, Bray F, Ferlay J, et al. Global cancer statistics, CA Cancer J Clin 2005;55: Bosch FX, Ribes J, Diaz M, et al. Primary liver cancer: worldwide incidence and trends. Gastroenterology 2004;127:S5 S Degos F, Christidis C, Ganne-Carrie N, et al. Hepatitis C virus related cirrhosis: time to occurrence of hepatocellular carcinoma and death. Gut 2000;47: Benvegnu L, Gios M, Boccato S, et al. Natural history of compensated viral cirrhosis: a prospective study on the incidence of hierarchy of major complications. Gut 2004;53: Sangiovanni A, Prati GM, Fasani P, et al. The natural history of compensated cirrhosis due to hepatitis C virus: a 17 year cohort study of 214 patients. Hepatology 2006;43: El-Serag HB, Mason AC. Rising incidence of hepatocellular carcinoma in the United States. 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7 806 MALIK ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 7, No. 7 risk: a Danish record-linkage study. Eur J Cancer 1994;30: Wolk A, Gridley G, Svensson M, et al. A prospective study of obesity and cancer risk (Sweden). Cancer Causes Control 2001; 12: Oh SW, Yoon YS, Shin SA. Effects of excess weight on cancer incidences depending on cancer sites and histological findings among men: Korea National Health Insurance Corporation Study. J Clin Oncol 2005;23: Ioannou GN, Splan MF, Weiss NS, et al. Incidence and predictors of hepatocellular carcinoma in patients with cirrhosis. Clin Gastroenterol Hepatol 2007;5: Yang S, Lin HZ, Hwang J, et al. Hepatic hyperplasia in noncirrhotic fatty liver: is obesity-related hepatic steatosis a premalignant condition? Cancer Res 2001;61: Bugianesi E. Non-alcoholic steatohepatitis and cancer. Clin Liver Dis 2007;11: del Olmo JA, Serra MA, Rodriguez F, et al. Incidence and risk factors for hepatocellular carcinoma in 967 patients with cirrhosis. J Cancer Res Clin Oncol 1998;124: Fattovich G, Stroffolini T, Zagni I, et al. Hepatocellular carcinoma in cirrhosis: incidence and risk factors. Gastroenterology 2004; 127:S35 S Zaman SN, Melia WM, Johnson RD, et al. Risk factors in development of hepatocellular carcinoma in cirrhosis: prospective study of 613 patients. Lancet 1985;1: Caroli-Bottino A, Nascimento CM, Basto S, et al. Hepatocellular carcinoma: incidental finding in cirrhotic explants livers. Transplant Proc 2005;37: Marsh JW, Dvorchik I, Subotin M, et al. The prediction of risk of recurrence and time to recurrence of hepatocellular carcinoma after orthotopic liver transplantation: a pilot study. Hepatology 1997;26: Roayaie S, Schwartz JD, Sung MW, et al. Recurrence of hepatocellular carcinoma after liver transplant: patterns and prognosis. Liver Transpl 2004;10: Chan EY, Larson AM, Fix OK, et al. Identifying risk for recurrent hepatocellular carcinoma after liver transplantation: implications for surveillance studies and new adjuvant therapies. Liver Transpl 2008;14: Reprint requests Address requests for reprints to: Shahid M. Malik, MD, Division of Gastroenterology, Hepatology and Nutrition, Suite 900, 3471 Fifth Avenue, Pittsburgh, Pennsylvania maliks@upmc.edu; fax: (412) Conflicts of interest The authors disclose no conflicts.
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