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Hepatocellular Carcinoma in the Absence of Cirrhosis in United States Veterans Is Associated With Nonalcoholic Fatty Liver Disease
Open accessAbstract
Background & aims Hepatocellular carcinoma (HCC) can develop in individuals without cirrhosis. We investigated risk factors for development of HCC in the absence of cirrhosis in a U.S.Methods We identified a national cohort of 1500 patients with verified HCC during 2005 to 2010 in the U.S. Veterans Administration (VA) and reviewed their full VA medical records for evidence of cirrhosis and risk factors for HCC. Patients without cirrhosis were assigned to categories of level 1 evidence for no cirrhosis (very high probability) or level 2 evidence for no cirrhosis (high probability), which were based on findings from histologic analyses, laboratory test results, markers of fibrosis from noninvasive tests, and imaging features.Results A total of 43 of the 1500 patients with HCC (2.9%) had level 1 evidence for no cirrhosis, and 151 (10.1%) had level 2 evidence for no cirrhosis; the remaining 1203 patients (80.1%) had confirmed cirrhosis. Compared with patients with HCC in presence of cirrhosis, greater proportions of patients with HCC without evidence of cirrhosis had metabolic syndrome, nonalcoholic fatty liver disease (NAFLD), or no identifiable risk factors. Patients with HCC without evidence of cirrhosis were less likely to have abused alcohol or have hepatitis C virus infection than patients with cirrhosis. Patients with HCC and NAFLD (unadjusted odds ratio, 5.4; 95% confidence interval, 3.4-8.5) or metabolic syndrome (unadjusted odds ratio, 5.0; 95% confidence interval, 3.1-7.8) had more than 5-fold risk of having HCC in the absence of cirrhosis, compared with patients with HCV-related HCC.Conclusions Approximately 13% of patients with HCC in the VA system do not appear to have cirrhosis. NAFLD and metabolic syndrome are the main risk factors for HCC in the absence of cirrhosis.
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“In the same cohort, the risk of HCC in the absence of cirrhosis was 5-fold higher in individuals with MASLD than in those with chronic hepatitis C.”
From EASL-EASD-EASO Clinical Practice Guidelines on the management of metabolic dysfunction-associated steatotic liver disease (MASLD). (2024) · cites this paper as [123]
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“Although HCC may develop in non-cirrhotic MASLD, cirrhosis remains the key risk factor for HCC.”
From EASL-EASD-EASO Clinical Practice Guidelines on the management of metabolic dysfunction-associated steatotic liver disease (MASLD). (2024) · cites this paper as [123]
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“In a US Veterans Administration cohort 123 including 1,500 individuals with HCC from 2005 to 2010, metabolic syndrome was particularly prevalent in the subgroup who had no cirrhosis.”
From EASL-EASD-EASO Clinical Practice Guidelines on the management of metabolic dysfunction-associated steatotic liver disease (MASLD). (2024) · cites this paper as [123]
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“the Veteran Administration reports incidence values around 13%.(11)”
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“Among new HCC cases without advanced fibrosis or cirrhosis, NAFLD is constitutes the largest etiological proportion of cases.(6) This entity poses a challenge to our clinical practice paradigms that are based on HCC risk mediated through cirrhosis, as well as our understanding of HCC pathogenesis.”
BackgroundEpidemiology and Risk Factors of Hepatocellular Carcinoma
El‐Serag, H. B., Balakrishnan, M., & Natarajan, Y. (2024) · Wiley eBooks · doi:10.1002/9781119756422.ch14 · Cited by 13
Yin, J., Zhu, Y., Liu, R., Wang, W., Wang, Z., & Wang, J. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1599956 · Cited by 12
Barrientos‐Riosalido, A., Real, M., Bertran, L., Aguilar, C., Martínez, S., Parada, D., Vives, M., Sabench, F., Riesco, D., Castillo, D. D., et al. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24021324 · Cited by 12
Prevention of liver cancer in the era of next-generation antivirals and obesity epidemic
Suzuki, H., Fujiwara, N., Singal, A. G., Baumert, T. F., Chung, R. T., Kawaguchi, T., & Hoshida, Y. (2025) · Hepatology · doi:10.1097/hep.0000000000001227 · Cited by 11
The importance of patient engagement in the multimodal treatment of MASLD
Boeckmans, J., Hagström, H., Cryer, D. R. H., & Schattenberg, J. M. (2025) · Communications Medicine · doi:10.1038/s43856-025-00871-1 · Cited by 16
Pan, M., Deng, Y., Zheng, C., Nie, H., Tang, K., Zhang, Y., & Yang, Q. (2019) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2019/8479680 · Cited by 11
“It encompasses a wide spectrum of conditions ranging from simple steatosis to nonalcoholic steatohepatitis (NASH) and may progress to advanced liver cirrhosis and hepatocellular carcinoma (HCC) [1, 2].”
BackgroundHydes, T., Cuthbertson, D. J., Graef, S., Berhane, S., Teng, M. J., Skowrońska, A., Singh, P., Dhanaraj, S., Tahrani, A. A., & Johnson, P. J. (2022) · Clinical Therapeutics · doi:10.1016/j.clinthera.2021.12.011 · Cited by 11
Hepatocellular Carcinoma Chemoprevention with Generic Agents
Rasha, F. A., Paul, S., Simon, T. G., & Hoshida, Y. (2022) · Seminars in Liver Disease · doi:10.1055/a-1942-6693 · Cited by 11
Type 2 diabetes complications are associated with liver fibrosis independent of hemoglobin A1c
Trivedi, H. D., Tran, Q., Fricker, Z. P., Curry, M. P., Li, J. X., & Lai, M. (2023) · Annals of Hepatology · doi:10.1016/j.aohep.2023.101087 · Cited by 11
Stroffolini, T., Sagnelli, E., Sagnelli, C., Morisco, F., Babudieri, S., Furlan, C., Pirisi, M., Russello, M., Smedile, A., Pisaturo, M., et al. (2019) · Infection · doi:10.1007/s15010-019-01308-3 · Cited by 12
Screening for Hepatocellular Carcinoma in HIV-Infected Patients: Current Evidence and Controversies
Merchante, N., Rodríguez-Fernández, M., & Pineda, J. A. (2020) · Current HIV/AIDS Reports · doi:10.1007/s11904-019-00475-0 · Cited by 12
Tayyab, G. U. N., Rasool, S., Nasir, B., Rubi, G., Abou‐Samra, A., & Butt, A. A. (2020) · BMC Gastroenterology · doi:10.1186/s12876-020-01249-4 · Cited by 11
Are, V. S., Gómez, E. V., Gromski, M. A., Akisik, F. M., Lammert, C. S., Ghabril, M., Chalasani, N., Vuppalanchi, R., & Nephew, L. D. (2021) · Liver International · doi:10.1111/liv.15008 · Cited by 11
Utilization of HCV viremic donors in kidney transplantation: a chance or a threat?
Czarnecka, P., Czarnecka, K., Tronina, O., Baczkowska, T., & Durlik, M. (2022) · Renal Failure · doi:10.1080/0886022x.2022.2047069 · Cited by 11
“Offering HCV-viremic organs to patients who are likely to have undiagnosed liver disease poses a threat of progression of liver disease, including hepatocellular carcinoma, which has been observed even in patients with NAFLD without evidence of cirrhosis [54].”
BackgroundXiong, G., Huang, C., Zou, Y., Tao, Z., Zou, J., & Huang, J. (2022) · Journal of Healthcare Engineering · doi:10.1155/2022/4912961 · Cited by 10
General Overview About the Current Management of Nonalcoholic Fatty Liver Disease
Ampuero, J. (2022) · Clinical Drug Investigation · doi:10.1007/s40261-022-01142-w · Cited by 10
S3-Leitlinie „Diagnostik und Therapie des Hepatozellulären Karzinoms“ – Langversion 4.0
Bitzer, M., Groß, S., Albert, J., Blödt, S., Boda‐Heggemann, J., Brunner, T. B., Caspari, R., Toni, E. D., Dombrowski, F., Evert, M., et al. (2024) · Zeitschrift für Gastroenterologie · doi:10.1055/a-2189-6353 · Cited by 10
Primary Sclerosing Cholangitis Limited to Intrahepatic Bile Ducts Has Distinctly Better Prognosis
Are, V. S., Gromski, M. A., Akisik, F. M., Vilar‐Gómez, E., Lammert, C. S., Ghabril, M., Vuppalanchi, R., & Chalasani, N. (2024) · Digestive Diseases and Sciences · doi:10.1007/s10620-023-08260-1 · Cited by 10
“The presence of cirrhosis at or before the date of entry and at the end of follow-up was determined based on Mittal criteria [17].”
Huang, M., Chen, H., Wang, H., Wang, X., Wang, D., Li, Y., Zhou, Q., Zhang, D., Li, M., & Ma, L. (2024) · Frontiers in Oncology · doi:10.3389/fonc.2024.1424155 · Cited by 10
NS 5 ABP 37 inhibits liver cancer by impeding lipogenesis and cholesterogenesis
Feng, S., Han, M., Zhou, L., Wang, Q., Li, Z., Li, Y., Lu, H., Liu, T., Ma, Y., Liu, S., et al. (2016) · Cancer Science · doi:10.1111/cas.13117 · Cited by 10
Zhang, Q., Chen, S., Ke, Y., Li, Q., Shen, C., Ruan, Y., Wu, K., Hu, J., & Liu, S. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1073498 · Cited by 11
Alomari, M., Rashid, M. U., Chadalavada, P. N., Ragheb, J. G., Zafar, H., Suarez, Z. K., Khazaaleh, S., Gonzalez, A. J., & Castro, F. (2023) · World Journal of Hepatology · doi:10.4254/wjh.v15.i4.477 · Cited by 11
Identification of ferroptosis-related genes in the progress of NASH
He, L., Wang, J., Tao, B., Zhu, R., Li, C., & Ning, B. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1184280 · Cited by 11
Epidemiological Trends in NASH as a Cause for Liver Transplant
Siow, W., van der Poorten, D., & George, J. (2016) · Current Hepatology Reports · doi:10.1007/s11901-016-0294-x · Cited by 10
Ciećko-Michalska, I., Szczepanek, M., Wierzbicka-Tutka, I., Zahradnik-Bilska, J., & Mach, T. (2018) · Archives of Medical Science - Atherosclerotic Diseases · doi:10.5114/amsad.2018.81184 · Cited by 10
“It has been demonstrated that HCC develops five times more often in liver without cirrhosis in patients with NAFLD than in other aetiologies [6].”
BackgrounddeLemos, A. S., Patel, M., Gawrieh, S., Burney, H. N., Dakhoul, L., Miller, E., Scanga, A. E., Kettler, C. D., Liu, H., Roche, P., et al. (2020) · Clinical and Translational Gastroenterology · doi:10.14309/ctg.0000000000000139 · Cited by 10
“1% noncirrhotic alcohol-related HCCs identified using the same criteria for the absence of cirrhosis (23).”
BackgroundDong, J., Liu, C., Lu, J., Wang, L., Xie, S., Ji, L., & Lu, B. (2023) · European Journal of Clinical Investigation · doi:10.1111/eci.14082 · Cited by 10
“2,4,5 Moreover, NAFLD has a serious impact on the global economic burden caused by public health problems.”
BackgroundYoon, C. H., Jin, Y., & Lee, J. W. (2018) · European Journal of Gastroenterology & Hepatology · doi:10.1097/meg.0000000000001174 · Cited by 10
Wen, Y., Lu, L., Mei, J., Ling, Y., Guan, R., Lin, W., Wei, W., & Guo, R. (2024) · Journal of Hepatocellular Carcinoma · doi:10.2147/jhc.s453250 · Cited by 9
Liver transplantation for non-alcoholic fatty liver disease—a review
Jayakumar, S. (2018) · AME Medical Journal · doi:10.21037/amj.2018.01.16 · Cited by 9
“Interestingly, HCC has been reported to occur in noncirrhotic NASH patients (20-22), thereby contributing to the increasing demand for LT through multiple mechanisms—CLD and HCC-related disease.”
BackgroundS3-Leitlinie: Diagnostik und Therapie des hepatozellulären Karzinoms
Voesch, S., Bitzer, M., Jörg, A., Bartenstein, P., Bechstein, W. O., Blödt, S., Thomas, B., Dombrowski, F., Evert, M., Follmann, M., et al. (2022) · Zeitschrift für Gastroenterologie · doi:10.1055/a-1589-7568 · Cited by 9
Fassio, E., Barreyro, F., Perez, M. S., Dávila, D., Landeira, G., Gualano, G., & Ruffillo, G. (2022) · World Journal of Hepatology · doi:10.4254/wjh.v14.i2.354 · Cited by 13
Metadata
- Authors
- Mittal, S., El-Serag, H. B., Sada, Y. H., Kanwal, F., Duan, Z., Temple, S., May, S. B., Kramer, J. R., Richardson, P. A., & Davila, J. A.
- Affiliations
- Michael E. DeBakey VA Medical Center (US)
- Corresponding author
- Mittal, Sahil
- Venue
- Clinical Gastroenterology and Hepatology
- Publisher
- Elsevier BV
- Published
- 2016-01
- Volume
- 14
- Issue
- 1
- Pages
- 124-131.e1
- ISSN
- 1542-3565 (ISSN-L)
- PMC
- PMC4690789
- OpenAlex
- W1258381707
- Cited by
- 648
- References
- 34
- Citations by year
- 2026: 27 · 2025: 63 · 2024: 61 · 2023: 64 · 2022: 77 · 2021: 99 · 2020: 85 · 2019: 60 · 2018: 47 · 2017: 41 · 2016: 19
- FWCI
- 22.09
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Clinical Gastroenterology and Hepatology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Cancer Institute (R01CA160738)
- Topics
- Health Sciences › Medicine › Hepatology › Hepatocellular Carcinoma Treatment and Prognosis
- Health Sciences › Medicine › Hepatology › Liver Disease Diagnosis and Treatment
- Health Sciences › Medicine › Hepatology › Liver physiology and pathology
- Keywords
- hepatocellular carcinoma, non-alcoholic fatty liver disease, liver cirrhosis, metabolic syndrome, risk factors, veterans, hepatitis C virus, alcohol abuse, liver fibrosis markers
- MeSH terms
- Aged, Aged, 80 and over, Female, Carcinoma, Hepatocellular, Humans, Male, Middle Aged, Risk Factors, United States, Veterans, Cohort Studies, Metabolic Syndrome, Non-alcoholic Fatty Liver Disease
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