Cited by 609Hepatocellular Carcinoma Treatment and PrognosisLiver Disease Diagnosis and TreatmentHead and Neck Cancer Studies

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Hepatocellular cancer: The impact of obesity, type 2 diabetes and a multidisciplinary team

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Dyson, Jessica, Jaques, Bryan, Chattopadyhay, Dipankar, Lochan, Rajiv, Graham, Janine, Das, Debasish, Aslam, Tahira, Patanwala, Imran, Gaggar, Sameer, Cole, Michael, Sumpter, Kate, Stewart, Stephen, Rose, John, Hudson, Mark, Manas, Derek, Reeves, Helen L.·2014·Journal of Hepatology

DOI 10.1016/j.jhep.2013.08.011

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Abstract

Background & aims Hepatocellular cancer (HCC) commonly complicates chronic liver disease and increases in incidence have been reported despite falling prevalences of viral hepatitis.Methods Following the introduction of centralised specialist teams to manage patients with cancer in England, we characterised the demographics of patients with HCC referred to the Newcastle-upon-Tyne Hospitals NHS Foundation Trust between 2000 and 2010. Regional HCC mortality data was from Public Health England.Results HCC related mortality in the region rose 1.8 fold in 10 years, from 2.0 to 3.7 per 100,000. 632 cases were reviewed centrally, with 2-3 fold increases in referrals of patients with associated hepatitis C, alcoholic liver disease or no chronic liver disease and a >10 fold increase in HCC associated with non-alcoholic fatty liver disease (NAFLD). By 2010 NAFLD accounted for 41/118 (34.8%) cases. Irrespective of associated etiologies, metabolic risk factors were present in 78/118 (66.1%) cases in 2010, associated with regional increases in obesity and diabetes. Median overall survival was just 10.7 months. Although patients with NAFLD associated HCC were older (71.3 yr vs. 67.1 yr; p<0.001) and their cancers less often detected by surveillance, their survival was similar to other etiologies. This was attributed to significantly higher incidental presentation (38.2%) and lower prevalence of cirrhosis (77.2%).Conclusions HCC related mortality is increasing, with typical patients being elderly with metabolic risk factors. The prognosis for most of the cases is poor, but older patients with co-morbidities can do well, managed, within a specialist multidisciplinary team if their cancer is detected pre-symptomatically.

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Background
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Influential
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Background
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Background
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Background
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Background
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ResultInfluential
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Background
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Background
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Result
Alpha-fetoprotein, protein induced by vitamin K absence or antagonist-II, lens culinaris agglutinin-reactive fraction of alpha-fetoprotein alone and in combination for early detection of hepatocellular carcinoma from nonalcoholic fatty liver disease: A multicenter analysis.
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Background
Role of B Lymphocytes in the Pathogenesis of NAFLD: A 2022 Update
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Background
The Changing Face of Hepatocellular Carcinoma: Forecasting Prevalence of Nonalcoholic Steatohepatitis and Hepatitis C Cirrhosis
Ahmed, O. S., Liu, L., Gayed, A., Baadh, A. S., Patel, M. V., Tasse, J., Turba, U. C., & Arslan, B. (2018) · Journal of Clinical and Experimental Hepatology · doi:10.1016/j.jceh.2018.02.006 · Cited by 27
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Result
Ethnic differences in hepatocellular carcinoma prevalence and therapeutic outcomes
Chavda, V. P., Zajac, K. K., Gunn, J., Balar, P. C., Khadela, A. D., Vaghela, D. A., Soni, S., Ashby, C. R., & Tiwari, A. K. (2023) · Cancer Reports · doi:10.1002/cnr2.1821 · Cited by 26
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Background
Extrahepatic comorbidities associated with hepatitis C virus in HIV-infected patients
Soriano, V., & Berenguer, J. (2015) · Current Opinion in HIV and AIDS · doi:10.1097/coh.0000000000000175 · Cited by 25
Controlled attenuation parameter reflects steatosis in compensated advanced chronic liver disease
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Emerging risk factors for nonalcoholic fatty liver disease associated hepatocellular carcinoma
Benhammou, J. N., Lin, J., Hussain, S. K., & El-Kabany, M. M. (2020) · Hepatoma Research · doi:10.20517/2394-5079.2020.16 · Cited by 25
A new nutraceutical (Livogen Plus®) improves liver steatosis in adults with non-alcoholic fatty liver disease
Ferro, Y., Pujia, R., Mazza, E., Lascala, L., Lodari, O., Maurotti, S., Pujia, A., & Montalcini, T. (2022) · Journal of Translational Medicine · doi:10.1186/s12967-022-03579-1 · Cited by 25
“Fatty liver disease could progress in non-alcoholic steatohepatitis (NASH), severe liver fibrosis, cirrhosis and hepatocellular cancer [4, 5].”
Background
Differential progression of unhealthy diet-induced hepatocellular carcinoma in obese and non-obese mice
Hymel, E., Vlock, E., Fisher, K., & Farazi, P. (2022) · PLoS ONE · doi:10.1371/journal.pone.0272623 · Cited by 20
Regorafenib: a promising treatment for hepatocellular carcinoma
Cerrito, L., Ponziani, F., Garcovich, M., Tortora, A., Annicchiarico, B., Pompili, M., Siciliano, M., & Gasbarrini, A. (2018) · Expert Opinion on Pharmacotherapy · doi:10.1080/14656566.2018.1534956 · Cited by 19
“The majority of HCC (90%) is associated to chronic liver disease and liver cirrhosis due to viral hepatitis (B and C infection), alcohol abuse, non-alcoholic fatty liver disease (NAFLD) [1,5,6].”
Background
Nonalcoholic fatty liver disease burden - Switzerland 2018-2030.
Goossens, N., Bellentani, S., Cerny, A., Dufour, J., Jornayvaz, F., Mertens, J., Moriggia, A., Muellhaupt, B., Negro, F., Razavi, H., et al. (2019) · Swiss medical weekly · doi:10.4414/smw.2019.20152 · Cited by 22
Shared Medical Appointments in Cancer Survivorship Care: A Review of the Literature
Reed, S. C., Partridge, A. H., & Nekhlyudov, L. (2015) · Journal of Oncology Practice · doi:10.1200/jop.2014.001411 · Cited by 24
Características clínicas del carcinoma hepatocelular en España. Comparación con el período 2008-2009 y análisis de las causas del diagnóstico fuera de cribado. Estudio de 686 casos en 73 centros
de Lope, C. R., Reig, M., Matilla, A. M., Ferrer, M. T., Dueñas, E., Mínguez, B., Castroagudı́n, J. F., Ortíz, I., Pascual, S., Lledó, J. L., et al. (2017) · Medicina Clínica · doi:10.1016/j.medcli.2016.12.048 · Cited by 26
FIB-4 index-based surveillance for advanced liver fibrosis in diabetes patients
Kawata, N., Takahashi, H., Iwane, S., Inoue, K., Kojima, M., Kohno, M., Tanaka, K., Mori, H., Isoda, H., Oeda, S., et al. (2020) · Diabetology International · doi:10.1007/s13340-020-00453-7 · Cited by 24
“In particular, according to the results of previous epidemiologic studies, abnormal glucose metabolism and diabetes are common lifestylerelated comorbidities of NAFLD, and are associated with the progression of liver fibrosis and the incidence of HCC [9, 10].”
Result
Evaluation of the Hepatorenal B-Mode Ratio and the “Controlled Attenuation Parameter” for the Detection and Grading of Steatosis
Moret, A., Boursier, J., Debry, P. H., Riou, J., Crouan, A., Dubois, M., Provost, S. M., Aubé, C., & Paisant, A. (2020) · Ultraschall in der Medizin - European Journal of Ultrasound · doi:10.1055/a-1233-2290 · Cited by 24
“Moreover, in this etiology hepatocellular carcinoma (HCC) could arise before the cirrhosis stage [2, 3].”
Background
Repeated measurements of non‐invasive fibrosis tests to monitor the progression of non‐alcoholic fatty liver disease: A long‐term follow‐up study
Balkhed, W., Åberg, F. O., Nasr, P., Ekstedt, M., & Kechagias, S. (2022) · Liver International · doi:10.1111/liv.15255 · Cited by 23
Effects of Bariatric Surgery on Non-alcoholic Fatty Liver Disease: Magnetic Resonance Imaging Is an Effective, Non-invasive Method to Evaluate Changes in the Liver Fat Fraction
Hedderich, D. M., Hasenberg, T., Haneder, S., Schoenberg, S. O., Kücükoglu, Ö., Canbay, A. E., & Otto, M. (2017) · Obesity Surgery · doi:10.1007/s11695-016-2531-3 · Cited by 24
Non-alcoholic steatohepatitis-related liver cirrhosis is increasing in China: A ten-year retrospective study
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Smad3 Phospho-Isoform Signaling in Nonalcoholic Steatohepatitis
Yamaguchi, T., Yoshida, K., Murata, M., Suwa, K., Tsuneyama, K., Matsuzaki, K., & Naganuma, M. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23116270 · Cited by 25
TLR4-Dependent Tumor-Initiating Stem Cell-Like Cells (TICs) in Alcohol-Associated Hepatocellular Carcinogenesis
Machida, K., Feldman, D. E., & Tsukamoto, H. (2014) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-09614-8_8 · Cited by 23
“These mechanisms may also be relevant to another etiological entity which promotes HCC risk: nonalcoholic fatty liver disease (NAFLD) [ 9 ] that is a liver phenotype of obesityassociated metabolic syndrome.”
Background
Hígado graso no alcohólico: una pandemia poco conocida
Augustín, S., Graupera, I., & Caballería, J. (2017) · Medicina Clínica · doi:10.1016/j.medcli.2017.06.026 · Cited by 23
Weighing the benefits of hepatocellular carcinoma surveillance against potential harms
Geh, D., Rana, F., & Reeves, H. (2019) · Journal of Hepatocellular Carcinoma · doi:10.2147/jhc.s159581 · Cited by 21
“Many of these patients present with advanced stage disease, where a lack of effective therapies contributes frequently to death within a year.(4) The term “surveillance” can be defined as the regular implementation of a diagnostic test to individuals at risk of developing a given disease.”
BackgroundInfluential
NAFLD-related HCC
Banini, B. A., & Sanyal, A. J. (2021) · Advances in cancer research · doi:10.1016/bs.acr.2020.11.001 · Cited by 21
NON-INVASIVE DIAGNOSIS AND FOLLOW-UP OF NON-ALCOHOLIC FATTY LIVER DISEASE.
Boursier, J., Guillaume, M., Bouzbib, C., Lannes, A., Pais, R., Smatti, S., Cariou, B., Bureau, C., Ganne-Carrié, N., Bourlière, M., et al. (2021) · Clinics And Research in Hepatology and Gastroenterology · doi:10.1016/j.clinre.2021.101769 · Cited by 21
Characterization of signature trends across the spectrum of non-alcoholic fatty liver disease using deep learning method
Park, I., Kim, N., Lee, S., Park, K., Son, M., Cho, H., & Kim, D. (2022) · Life Sciences · doi:10.1016/j.lfs.2022.121195 · Cited by 21
Should we undertake surveillance for HCC in patients with MAFLD?
Norero, B., & Dufour, J. (2023) · Therapeutic Advances in Endocrinology and Metabolism · doi:10.1177/20420188231160389 · Cited by 20
Anatomic versus non‐anatomic liver resection for hepatocellular carcinoma—A European multicentre cohort study in cirrhotic and non‐cirrhotic patients
Zeindler, J., Hess, G. F., von Heesen, M., Aegerter, N. L. E., Reber, C., Schmitt, A. M., Muenst, S. E., Bolli, M., Soysal, S. D., & Kollmar, O. (2024) · Cancer Medicine · doi:10.1002/cam4.6981 · Cited by 21
Practical approach to non‐alcoholic fatty liver disease in patients with diabetes
Tai, F. W. D., Syn, W., & Alazawi, W. (2015) · Diabetic Medicine · doi:10.1111/dme.12725 · Cited by 21
The Relationship of Diabetes and Smoking Status to Hepatocellular Carcinoma Mortality
Chiang, C., Lu, C., Han, H.-C., Hung, S.-H., Lee, Y., Yang, K., & Huang, K. (2016) · Medicine · doi:10.1097/md.0000000000002699 · Cited by 21
“8%) by 2010.(26) Although chronic viral hepatitis remains a major risk factor of HCC in Taiwan,(27,28) we have observed the association between certain viral factor, such as hepatitis B viral load and selected host metabolic factors.”
Background
Natural history of nonalcoholic steatohepatitis/nonalcoholic fatty liver disease‐hepatocellular carcinoma: Magnitude of the problem from a hepatology clinic perspective
D'Avola, D., Labgaa, I., & Villanueva, A. (2016) · Clinical Liver Disease · doi:10.1002/cld.579 · Cited by 21
The molecular basis for current targets of NASH therapies
Qureshi, K., & Neuschwander‐Tetri, B. A. (2019) · Expert Opinion on Investigational Drugs · doi:10.1080/13543784.2020.1703949 · Cited by 23
Prevalence of the Absence of Cirrhosis in Subjects with NAFLD-Associated Hepatocellular Carcinoma
Castellana, M., Donghia, R., Lampignano, L., Castellana, F., Zupo, R., Sardone, R., Pergola, G. D., & Giannelli, G. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10204638 · Cited by 20
“Dyson, 2014 [19] United Kingdom PCS 2000–2010 NAFLD 136 Gawrieh, 2019 [20] USA RCS 2000–2014 NAFLD 767 Hester, 2019 [21] USA RCS 2008–2016 NASH 92 Kanwal, 2018 [22] USA RCS 2003–2011 NAFLD 490 Kodama, 2019 [23] Japan RCS 2000–2016 NAFLD 104 Koh, 2019 [24] Singapore PCS 2000–2015 NAFLD 152 Leung, 2015 [25] Australia RC…”
Non-alcoholic fatty liver disease in adults 2021: A clinical practice guideline of the Italian Association for the Study of the Liver (AISF), the Italian Society of Diabetology (SID) and the Italian Society of Obesity (SIO)
Associazione Italiana per lo Studio del Fegato (AISF), S. I. D. D. (. A. S. I. D. (. (2021) · Eating and Weight Disorders - Studies on Anorexia Bulimia and Obesity · doi:10.1007/s40519-021-01287-1 · Cited by 22
“…an almost 7-fold increased risk of HCC compared to people without liver disease [49] and the risk is > 10 folds higher in association with T2DM and obesity [52] , making NAFLD the second leading cause of liver transplantation (LT) due to HCC in U.S and the most rapidly increasing indication [53] .”
Discriminatory Changes in Circulating Metabolites as a Predictor of Hepatocellular Cancer in Patients with Metabolic (Dysfunction) Associated Fatty Liver Disease
Lu, H., George, J., Eslam, M., Villanueva, A., Bolondi, L., Reeves, H. L., McCain, M. V., Chambers, E. S., Ward, C. E., Sartika, D., et al. (2022) · Liver Cancer · doi:10.1159/000525911 · Cited by 19
How to Diagnose Nonalcoholic Fatty Liver Disease
de Alwis, N. D., Anstee, Q., & Day, C. (2016) · Digestive Diseases · doi:10.1159/000447277 · Cited by 18
Multicentre study of the prognostic impact of preoperative bodyweight on long-term prognosis of hepatocellular carcinoma
Yu, J. J., Shen, F., Chen, T. H., Liang, L., Han, J. S., Xing, H., Zhou, Y. ‐., Wang, H., Gu, W. M., Lau, W. Y., et al. (2018) · British journal of surgery · doi:10.1002/bjs.10981 · Cited by 20
Targeting the Cholecystokinin Receptor: A Novel Approach for Treatment and Prevention of Hepatocellular Cancer
Gay, M. D., Safronenka, A., Cao, H., Liu, F. H., Malchiodi, Z. X., Tucker, R. D., Kroemer, A., Shivapurkar, N., & Smith, J. P. (2020) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-20-0220 · Cited by 20
“Although vaccination for hepatitis B and treatment of hepatitis C have helped to decrease the liver cancer incidence from viral etiologies, the new obesity pandemic associated with the rising prevalence of nonalcoholic steatohepatitis (NASH) has become a new risk factor for cirrhosis and HCC (6, 7).”
Background
The Current View of Nonalcoholic Fatty Liver Disease-Related Hepatocellular Carcinoma
Kogiso, T., & Tokushige, K. (2021) · Cancers · doi:10.3390/cancers13030516 · Cited by 20
“[34] 2014 632 HCC patients/2000–2010 Non-cirrhotic 31/136 (22.”
Circulating tumor cells detected with a microcavity array predict clinical outcome in hepatocellular carcinoma
Takahashi, K., Ofuji, K., Hiramatsu, K., Nosaka, T., Naito, T., Matsuda, H., Endo, K., Higuchi, M., Ohtani, M., Nemoto, T., et al. (2021) · Cancer Medicine · doi:10.1002/cam4.3790 · Cited by 20
Reply to: HCC and liver disease risk in homozygous PNPLA3 p.I148M carriers approach monogenic inheritance
Anstee, Q. M., Liu, Y., Day, C. P., & Reeves, H. L. (2015) · Journal of Hepatology · doi:10.1016/j.jhep.2014.12.028 · Cited by 20
The endocrine role of hepatokines: implications for human health and disease
Iglesias, P. (2025) · Frontiers in Endocrinology · doi:10.3389/fendo.2025.1663353 · Cited by 23
“Importantly, HCC in the context of NAFLD/ NASH may develop even in the absence of cirrhosis (83, 84), distinguishing it from traditional viral-or alcohol-related liver cancers.”
Impact of NAFLD on clinical outcomes in hepatocellular carcinoma treated with sorafenib: an international cohort study
Howell, J. A., Samani, A., Mannan, B., Hajiev, S., Aval, L. M., Abdelmalak, R., Tam, V. C., Bettinger, D., Thimme, R., Taddei, T. H., et al. (2022) · Therapeutic Advances in Gastroenterology · doi:10.1177/17562848221100106 · Cited by 19
NAFLD as the metabolic hallmark of obesity
Rojano‐Toimil, A., Sena, E., Manzano-Núñez, R., Pericàs, J. M., & Ciudin, A. (2022) · Internal and Emergency Medicine · doi:10.1007/s11739-022-03139-x · Cited by 22
“Indeed, for patients with NASH-related cirrhosis has been observed a > tenfold increase in risk for HCC [18].”
Background
The role of tumor microenvironment reprogramming in primary liver cancer chemotherapy resistance
Zhao, C., Liu, S., Gao, F., Zou, Y., Ren, Z., & Yu, Z. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.1008902 · Cited by 19
“However, other factors have also been implicated in the occurrence of HCC, including fatty liver disease, dietary aflatoxin exposure, alcohol-related cirrhosis, smoking, obesity, fatty liver disease, iron overload, Mellitusrelated non-alcoholic fatty liver disease and type 2 diabetes (3, 4).”
Background
Fibrosis-4 stage of liver fibrosis predicts cardiovascular outcomes in acute coronary syndrome patients with and without type 2 diabetes mellitus
Song, J., Liu, Y., Chen, J., Yang, J., Wen, J., Gao, J., Shao, C., Wang, W., & Tang, Y. (2022) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2022.110206 · Cited by 20
Screening for NAFLD—Current Knowledge and Challenges
Forlano, R., Sigon, G., Mullish, B. H., Yee, M. S., & Manousou, P. (2023) · Metabolites · doi:10.3390/metabo13040536 · Cited by 22
Beyond the Liver: A Comprehensive Review of Strategies to Prevent Hepatocellular Carcinoma
Polpichai, N., Saowapa, S., Danpanichkul, P., Chan, S., Sierra, L., Blagoie, J., Rattananukrom, C., Sripongpun, P., & Kaewdech, A. (2024) · Journal of Clinical Medicine · doi:10.3390/jcm13226770 · Cited by 25
“Obesity and metabolic syndrome are associated with MASLD, which can progress to metabolic dysfunction-associated steatohepatitis (MASH) and subsequently increase the risk of HCC [50].”
Back to Byzance: Querelles byzantines over NASH and fibrosis
Ratziu, V. (2017) · Journal of Hepatology · doi:10.1016/j.jhep.2017.09.024 · Cited by 19
Reduction of Polyunsaturated Fatty Acids with Tumor Progression in a Lean Non-Alcoholic Steatohepatitis-Associated Hepatocellular Carcinoma Mouse Model
Vlock, E., Karanjit, S., Talmon, G., & Farazi, P. (2020) · Journal of Cancer · doi:10.7150/jca.48495 · Cited by 18
“Furthermore, mRNA sequencing analysis revealed lower expression of genes implicated in desaturase expression such as Srebf1, Scap, Fasn, and Acly in HCCs compared to livers with NAFLD.”
BackgroundInfluential

Authors: Dyson, J., Jaques, B., Chattopadyhay, D., Lochan, R., Graham, J., Das, D., Aslam, T., Patanwala, I., Gaggar, S., Cole, M., Sumpter, K., Stewart, S., Rose, J., Hudson, M., Manas, D., & Reeves, H. L.
Affiliations: Newcastle upon Tyne Hospitals NHS Foundation Trust (GB)
Newcastle University (GB)
Corresponding author: Reeves, Helen L.
ORCID: Dyson, Jessica
Das, Debasish
Patanwala, Imran
Cole, Michael
Stewart, Stephen
Hudson, Mark
Manas, Derek
Reeves, Helen L.
Venue: Journal of Hepatology
Publisher: Elsevier BV
Published: 2014-01
Volume: 60
Issue: 1
Pages: 110-117
ISSN: 0168-8278 (ISSN-L)
DOI: 10.1016/j.jhep.2013.08.011
OpenAlex: W2076341209
Cited by: 603
References: 25
Citations by year: 2026: 23 · 2025: 32 · 2024: 45 · 2023: 43 · 2022: 72 · 2021: 65 · 2020: 63 · 2019: 60 · 2018: 57 · 2017: 48 · 2016: 38 · 2015: 33 · 2014: 18
FWCI: 19.26
Type: journal article
Language: en
Open access: green
zenodo.org
Licence: other-oa
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Journal of Hepatology (publishedVersion)
PubMed (publishedVersion)
Zenodo (CERN European Organization for Nuclear Research) (submittedVersion, other-oa)
Newcastle University ePrints (Newcastle Univesity)
Topics: Health Sciences › Medicine › Hepatology › Hepatocellular Carcinoma Treatment and Prognosis
Health Sciences › Medicine › Hepatology › Liver Disease Diagnosis and Treatment
Health Sciences › Medicine › Otorhinolaryngology › Head and Neck Cancer Studies
Keywords: hepatocellular carcinoma, obesity, type 2 diabetes, non-alcoholic fatty liver disease, HCC mortality, chronic liver disease, hepatitis C, alcoholic liver disease, metabolic risk factors, multidisciplinary cancer care, cancer surveillance, liver cirrhosis, overall survival, cancer incidence trends
MeSH terms: Age Factors, Aged, Diabetes Mellitus, Type 2, Fatty Liver, Humans, Liver Neoplasms, Middle Aged, Obesity, Risk Factors, Non-alcoholic Fatty Liver Disease

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Hepatocellular cancer: The impact of obesity, type 2 diabetes and a multidisciplinary team

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