CoChat
Sign Up
Cited by 177Cancer Risks and FactorsHepatocellular Carcinoma Treatment and PrognosisLiver Disease Diagnosis and Treatment

Obesity and the risk of primary liver cancer: A systematic review and meta-analysis

Open access
Sohn, Won, Lee, Hyun Woong, Lee, Sangheun, Lim, Jin Hong, Lee, Min Woo, Park, Chan Hyuk, Yoon, Seung Kew·2021·Clinical and Molecular Hepatology
DOI 10.3350/cmh.2020.0176PMC PMC7820201
Open this paper in CoChat — free accountOpen PDF

Abstract

Background/Aims: In this systematic review and meta-analysis, we aimed to clarify the effect of obesity on the occurrence of and mortality from primary liver cancer.Methods: This study was conducted using a systematic literature search of MEDLINE, EMBASE, and the Cochrane Library until November 2018 using the primary keywords “obesity,” “overweight,” “body mass index (BMI),” “body weight,” “liver,” “cancer,” “hepatocellular carcinoma,” “liver cancer,” “risk,” and “mortality.” Studies assessing the relationship between BMI and occurrence of or mortality from primary liver cancer in prospective cohorts and those reporting hazard ratios (HRs) or data that allow HR estimation were included.Results: A total of 28 prospective cohort studies with 8,135,906 subjects were included in the final analysis. These included 22 studies with 6,059,561 subjects for cancer occurrence and seven studies with 2,077,425 subjects for cancerrelated mortality. In the meta-analysis, an increase in BMI was associated with the occurrence of primary liver cancer (HR, 1.69; 95% confidence interval, 1.50–1.90, I 2=56%). A BMI-dependent increase in the risk of occurrence of primary liver cancer was reported. HRs were 1.36 (95% CI, 1.02–1.81), 1.77 (95% CI, 1.56–2.01), and 3.08 (95% CI, 1.21–7.86) for BMI >25 kg/m 2, >30 kg/m 2, and >35 kg/m 2, respectively. Furthermore, increased BMI resulted in enhanced liver cancer-related mortality (HR, 1.61; 95% CI, 1.14–2.27, I 2=80%).Conclusions: High BMI increases liver cancer mortality and occurrence of primary liver cancer. Obesity is an independent risk factor for the occurrence of and mortality from primary liver cancer.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3350/cmh.2020.0176

Cites

7 of 7 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • High BMI is associated with an increased risk of colorectal cancer, primary liver cancer, and cancer mortality.

    “High BMI is also associated with an increased risk of colorectal cancer [15], primary liver cancer, and cancer mortality [16].”

    From Advantages and Limitations of the Body Mass Index (BMI) to Assess Adult Obesity (2024) · cites this paper as [16]

    The Results report that higher BMI is associated with primary liver cancer occurrence and liver cancer-related mortality. Citation [16] supports the primary liver cancer claim, but the paper's mortality finding is specific to liver cancer, not cancer mortality generally. The colorectal cancer claim is attached to [15], not this source. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 50

  1. [1]Hruby A Hu FB The epidemiology of obesity: a big picture Pharmacoeconomics 2015 33 673 689 25471927 PMC4859313
  2. [4]Goodwin PJ Stambolic V Impact of the obesity epidemic on cancer Annu Rev Med 2015 66 281 296 25423596
  3. [5]Parekh N Chandran U Bandera EV Obesity in cancer survival Annu Rev Nutr 2012 32 311 342 22540252 PMC3807693
  4. [6]Wong MC Jiang JY Goggins WB Liang M Fang Y Fung FD International incidence and mortality trends of liver cancer: a global profile Sci Rep 2017 7 45846 28361988 PMC5374459
  5. [7]Llovet JM Zucman-Rossi J Pikarsky E Sangro B Schwartz M Sherman M Hepatocellular carcinoma Nat Rev Dis Primers 2016 2 16018 27158749
  6. [8]Ratziu V Bonyhay L Di Martino V Charlotte F Cavallaro L Sayegh-Tainturier MH Survival, liver failure, and hepatocellular carcinoma in obesity-related cryptogenic cirrhosis Hepatology 2002 35 1485 1493 12029634
  7. [9]Ohki T Tateishi R Sato T Masuzaki R Imamura J Goto T Obesity is an independent risk factor for hepatocellular carcinoma development in chronic hepatitis C patients Clin Gastroenterol Hepatol 2008 6 459 464 18387499
  8. [10]Chen CL Yang HI Yang WS Liu CJ Chen PJ You SL Metabolic factors and risk of hepatocellular carcinoma by chronic hepatitis B/C infection: a follow-up study in Taiwan Gastroenterology 2008 135 111 121 18505690
  9. [11]Chen Y Wang X Wang J Yan Z Luo J Excess body weight and the risk of primary liver cancer: an updated meta-analysis of prospective studies Eur J Cancer 2012 48 2137 2145 22446023
  10. [12]Rui R Lou J Zou L Zhong R Wang J Xia D Excess body mass index and risk of liver cancer: a nonlinear dose-response meta-analysis of prospective studies PLoS One 2012 7 e44522 23028553 PMC3445525
  11. [13]Wang Y Wang B Shen F Fan J Cao H Body mass index and risk of primary liver cancer: a meta-analysis of prospective studies Oncologist 2012 17 1461 1468 22956536 PMC3500368
  12. [14]Stang A Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses Eur J Epidemiol 2010 25 603 605 20652370
  13. [15]Castillo JJ Mull N Reagan JL Nemr S Mitri J Increased incidence of non-Hodgkin lymphoma, leukemia, and myeloma in patients with diabetes mellitus type 2: a meta-analysis of observational studies Blood 2012 119 4845 4850 22496152 PMC3367891
  14. [16]Singh S Singh PP Singh AG Murad MH Sanchez W Statins are associated with a reduced risk of hepatocellular cancer: a systematic review and meta-analysis Gastroenterology 2013 144 323 332 23063971
  15. [17]Park CH Kim EH Roh YH Kim HY Lee SK The association between the use of proton pump inhibitors and the risk of hypomagnesemia: a systematic review and meta-analysis PLoS One 2014 9 e112558 25394217 PMC4230950
  16. [18]DerSimonian R Laird N Meta-analysis in clinical trials Control Clin Trials 1986 7 177 188 3802833
  17. [19]Higgins JP Thompson SG Deeks JJ Altman DG Measuring inconsistency in meta-analyses BMJ 2003 327 557 560 12958120 PMC192859
  18. [20]Egger M Davey Smith G Schneider M Minder C Bias in meta-analysis detected by a simple, graphical test BMJ 1997 315 629 634 9310563 PMC2127453
  19. [24]Calle EE Rodriguez C Walker-Thurmond K Thun MJ Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults N Engl J Med 2003 348 1625 1638 12711737
  20. [25]Batty GD Shipley MJ Jarrett RJ Breeze E Marmot MG Smith GD Obesity and overweight in relation to organ-specific cancer mortality in London (UK): findings from the original Whitehall study Int J Obes (Lond) 2005 29 1267 1274 15997248
  21. [26]Kuriyama S Tsubono Y Hozawa A Shimazu T Suzuki Y Koizumi Y Obesity and risk of cancer in Japan Int J Cancer 2005 113 148 157 15386435
  22. [27]Rapp K Schroeder J Klenk J Stoehr S Ulmer H Concin H Obesity and incidence of cancer: a large cohort study of over 145,000 adults in Austria Br J Cancer 2005 93 1062 1067 16234822 PMC2361672
  23. [28]N’Kontchou G Paries J Htar MT Ganne-Carrie N Costentin L Grando-Lemaire V Risk factors for hepatocellular carcinoma in patients with alcoholic or viral C cirrhosis Clin Gastroenterol Hepatol 2006 4 1062 1068 16844421
  24. [29]Jee SH Yun JE Park EJ Cho ER Park IS Sull JW Body mass index and cancer risk in Korean men and women Int J Cancer 2008 123 1892 1896 18651571
  25. [30]Joshi S Song YM Kim TH Cho SI Socio-economic status and the risk of liver cancer mortality: a prospective study in Korean men Public Health 2008 122 1144 1151 18793784
  26. [31]Inoue M Kurahashi N Iwasaki M Tanaka Y Mizokami M Noda M Metabolic factors and subsequent risk of hepatocellular carcinoma by hepatitis virus infection status: a large-scale population-based cohort study of Japanese men and women (JPHC Study Cohort II) Cancer Causes Control 2009 20 741 750 19115074
  27. [32]Wang CS Yao WJ Chang TT Wang ST Chou P The impact of type 2 diabetes on the development of hepatocellular carcinoma in different viral hepatitis statuses Cancer Epidemiol Biomarkers Prev 2009 18 2054 2060 19549812
  28. [33]Hart CL Batty GD Morrison DS Mitchell RJ Smith GD Obesity, overweight and liver disease in the Midspan prospective cohort studies Int J Obes (Lond) 2010 34 1051 1059 20142829 PMC2887083
  29. [34]Chao LT Wu CF Sung FY Lin CL Liu CJ Huang CJ Insulin, glucose and hepatocellular carcinoma risk in male hepatitis B carriers: results from 17-year follow-up of a population-based cohort Carcinogenesis 2011 32 876 881 21464041 PMC3146359
  30. [35]Hung CH Lee CM Wang JH Hu TH Chen CH Lin CY Impact of diabetes mellitus on incidence of hepatocellular carcinoma in chronic hepatitis C patients treated with interferon-based antiviral therapy Int J Cancer 2011 128 2344 2352 20669224
  31. [37]Chen CT Chen JY Wang JH Chang KC Tseng PL Kee KM Diabetes mellitus, metabolic syndrome and obesity are not significant risk factors for hepatocellular carcinoma in an HBV- and HCV-endemic area of Southern Taiwan Kaohsiung J Med Sci 2013 29 451 459 23906236 PMC11916133
  32. [38]Li Y Yatsuya H Yamagishi K Wakai K Tamakoshi A Iso H Body mass index and weight change during adulthood are associated with increased mortality from liver cancer: the JACC Study J Epidemiol 2013 23 219 226 23604063 PMC3700251
  33. [40]Song X Pukkala E Dyba T Tuomilehto J Moltchanov V Männistö S Body mass index and cancer incidence: the FINRISK study Eur J Epidemiol 2014 29 477 487 24997743
  34. [41]Meyer J Rohrmann S Bopp M Faeh D Swiss National Cohort Study Group Impact of smoking and excess body weight on overall and site-specific cancer mortality risk Cancer Epidemiol Biomarkers Prev 2015 24 1516 1522 26215293
  35. [42]Campbell PT Newton CC Freedman ND Koshiol J Alavanja MC Beane Freeman LE Body mass index, waist circumference, diabetes, and risk of liver cancer for U.S. adults Cancer Res 2016 76 6076 6083 27742674 PMC5141518
  36. [43]Liu Y Warren Andersen S Wen W Gao YT Lan Q Rothman N Prospective cohort study of general and central obesity, weight change trajectory and risk of major cancers among Chinese women Int J Cancer 2016 139 1461 1470 27177094 PMC5020699
  37. [44]Setiawan VW Lim U Lipworth L Lu SC Shepherd J Ernst T Sex and ethnic differences in the association of obesity with risk of hepatocellular carcinoma Clin Gastroenterol Hepatol 2016 14 309 316 26404865 PMC4718778
  38. [45]McMahon BJ Bruden D Townshend-Bulson L Simons B Spradling P Livingston S Infection with hepatitis C virus genotype 3 is an independent risk factor for end-stage liver disease, hepatocellular carcinoma, and liver-related death Clin Gastroenterol Hepatol 2017 15 431 437 e2 27765729 PMC5316337
  39. [46]Nderitu P Bosco C Garmo H Holmberg L Malmström H Hammar N The association between individual metabolic syndrome components, primary liver cancer and cirrhosis: a study in the Swedish AMORIS cohort Int J Cancer 2017 141 1148 1160 28577304
  40. [47]Yang B Petrick JL Kelly SP Graubard BI Freedman ND McGlynn KA Adiposity across the adult life course and incidence of primary liver cancer: the NIH-AARP cohort Int J Cancer 2017 141 271 278 28411388 PMC5491533
  41. [48]Brichler S Nahon P Zoulim F Layese R Bourcier V Audureau E Non-virological factors are drivers of hepatocellular carcinoma in virosuppressed hepatitis B cirrhosis: results of ANRS CO12 CirVir cohort J Viral Hepat 2019 26 384 396 30380181
  42. [49]Hagström H Tynelius P Rasmussen F High BMI in late adolescence predicts future severe liver disease and hepatocellular carcinoma: a national, population-based cohort study in 1.2 million men Gut 2018 67 1536 1542 28320770
  43. [50]Jeong SH Kim P Yi SW Kim YJ Baeg MK Yi JJ Body mass index and gastrointestinal cancer mortality in Korean adults: a prospective cohort study J Gastroenterol Hepatol 2018 33 1582 1589 29406580
  44. [51]Yi SW Choi JS Yi JJ Lee YH Han KJ Risk factors for hepatocellular carcinoma by age, sex, and liver disorder status: a prospective cohort study in Korea Cancer 2018 124 2748 2757 29669170
  45. [53]Park EJ Lee JH Yu GY He G Ali SR Holzer RG Dietary and genetic obesity promote liver inflammation and tumorigenesis by enhancing IL-6 and TNF expression Cell 2010 140 197 208 20141834 PMC2836922
  46. [54]Larsson SC Wolk A Overweight, obesity and risk of liver cancer: a meta-analysis of cohort studies Br J Cancer 2007 97 1005 1008 17700568 PMC2360408
  47. [55]Pollak M Insulin and insulin-like growth factor signalling in neoplasia Nat Rev Cancer 2008 8 915 928 19029956
  48. [57]McGlynn KA Petrick JL London WT Global epidemiology of hepatocellular carcinoma: an emphasis on demographic and regional variability Clin Liver Dis 2015 19 223 238 25921660 PMC4712629
  49. [58]WHO Expert Consultation Appropriate body-mass index for Asian populations and its implications for policy and intervention strategies Lancet 2004 363 157 163 14726171
  50. [59]Yi SW Hong JS Yi JJ Ohrr H Impact of alcohol consumption and body mass index on mortality from nonneoplastic liver diseases, upper aerodigestive tract cancers, and alcohol use disorders in Korean older middle-aged men: prospective cohort study Medicine (Baltimore) 2016 95 e4876 27684819 PMC5265912

Cited by

Sorted by citations

Authors
Sohn, W., Lee, H. W., Lee, S., Lim, J. H., Lee, M. W., Park, C. H., & Yoon, S. K.
Affiliations
  • Kangbuk Samsung Hospital (KR)
  • Yonsei University (KR)
  • Catholic Kwandong University International St. Mary's Hospital (KR)
  • Samsung Medical Center (KR)
  • Hanyang University Guri Hospital (KR)
  • The Catholic University of Korea Seoul St. Mary's Hospital (KR)
Corresponding author
Yoon, Seung Kew
ORCID
Venue
Clinical and Molecular Hepatology
Publisher
The Korean Association for the Study of the Liver
Published
2021-01-01
Volume
27
Issue
1
Pages
157-174
ISSN
  • 2287-2728 (ISSN-L)
  • 2287-285X
DOI
10.3350/cmh.2020.0176
PMC
PMC7820201
OpenAlex
W3107494356
Cited by
177
References
7
Citations by year
2026: 21 · 2025: 32 · 2024: 47 · 2023: 41 · 2022: 24 · 2021: 9 · 2020: 1 · 2016: 1
FWCI
2.01
Type
journal article
Language
en
Open access
Licence
Locations
  • Clinical and Molecular Hepatology (publishedVersion, cc-by-nc)
  • Europe PMC (PubMed Central) (publishedVersion, other-oa)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • YUHSpace (Yonsei University Medical Library) (submittedVersion, cc-by-nc-nd)
Funders
  • Korea University Guro Hospital
  • Seoul National University
  • Soonchunhyang University
  • University of Ulsan
  • Yonsei University
  • Korea University
  • Sungkyunkwan University
  • Catholic University of Korea
  • Seoul National University Hospital
  • Samsung
  • College of Medicine, Seoul National University
  • College of Medicine, Catholic University of Korea
Topics
  • Health Sciences › Medicine › Oncology › Cancer Risks and Factors
  • Health Sciences › Medicine › Hepatology › Hepatocellular Carcinoma Treatment and Prognosis
  • Health Sciences › Medicine › Epidemiology › Liver Disease Diagnosis and Treatment
Keywords
obesity, primary liver cancer, hepatocellular carcinoma, body mass index, overweight, cancer risk, cancer mortality, risk factors
MeSH terms
Humans, Liver Neoplasms, Male, Obesity, Prospective Studies, Risk Factors, Body Mass Index, Overweight

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review