Skip to main content
SpringerLink
Log in

Cohort Contributions to Race- and Gender-Specific Trends in the Incidence of Hepatocellular Carcinoma in the USA

  • Original Scientific Report
  • Published:
World Journal of Surgery Aims and scope Submit manuscript

Abstract

Introduction

Increasing incidence of lifelong obesity and associated nonalcoholic steatohepatitis in younger birth cohorts may have contributed to growing incidence of hepatocellular carcinoma (HCC) in the USA. Yet, the contribution of cohort effects to trends in HCC incidence is unclear.

Methods

Using data from the Surveillance, Epidemiology, and End Results (SEER) program 1973–2013, race- and gender-specific trends in HCC incidence in the USA were decomposed using age-period-cohort (APC) modeling.

Results

Among SEER registry sites included in the analysis, there were 25,532 cases of HCC diagnosed including 15,867 (62%) White males, 3541 (14%) Black males, 5009 (20%) White females, and 1115 (4%) Black females. HCC incidence increases across periods, especially among men. Underlying this increase, APC models found significant cohort effects among White men, White women, and Black men, with rapid growth in HCC risk among cohorts born after 1940. A similar cohort trend among Black women did not reach statistical significance when compared to an age-period model.

Conclusions

Cohort-specific trends have significantly contributed to increasing HCC incidence in recent decades. The rapid increase in HCC risk among younger cohorts suggests that the incidence of HCC will continue increasing in the near future.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

ALD:

Alcoholic liver disease

APC:

Age-period-cohort

HCC:

Hepatocellular carcinoma

HBV:

Hepatitis B virus

HCV:

Hepatitis C virus

MELD:

Model for end stage liver disease

NASH:

Nonalcoholic steatohepatitis

NAFLD:

Nonalcoholic fatty liver disease

References

  1. El-Serag HB (2011) Hepatocellular carcinoma. N Engl J Med 365:1118–1127

    Article  CAS  PubMed  Google Scholar 

  2. Schütte K, Bornschein J, Malfertheiner P (2009) Hepatocellular carcinoma–epidemiological trends and risk factors. Dig Dis 27:80–92

    PubMed  Google Scholar 

  3. White DL, Thrift AP, Kanwal F et al (2017) Incidence of hepatocellular carcinoma in all 50 United States, from 2000 through 2012. Gastroenterology 152(812–820):e815

    Google Scholar 

  4. Altekruse SF, Henley SJ, Cucinelli JE, McGlynn KA (2014) Changing hepatocellular carcinoma incidence and liver cancer mortality rates in the United States. Am J Gastroenterol 109:542–553

    Article  PubMed  PubMed Central  Google Scholar 

  5. Petrick JL, Kelly SP, Altekruse SF et al (2016) Future of hepatocellular carcinoma incidence in the United States forecast through 2030. J Clin Oncol 34:1787–1794

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Gritsenko D, Hughes G (2015) Ledipasvir/Sofosbuvir (harvoni): improving options for hepatitis C virus infection. P T 40:256–276

    PubMed  PubMed Central  Google Scholar 

  7. Yonghao G, Jin X, Jun L et al (2015) An epidemiological serosurvey of hepatitis B virus shows evidence of declining prevalence due to hepatitis B vaccination in central China. Int J Infect Dis 40:75–80

    Article  PubMed  Google Scholar 

  8. Bhatnagar-Mathur P, Sunkara S, Bhatnagar-Panwar M et al (2015) Biotechnological advances for combating Aspergillus flavus and aflatoxin contamination in crops. Plant Sci 234:119–132

    Article  CAS  PubMed  Google Scholar 

  9. Wong RJ, Aguilar M, Cheung R et al (2015) Nonalcoholic steatohepatitis is the second leading etiology of liver disease among adults awaiting liver transplantation in the United States. Gastroenterology 148:547–555

    Article  PubMed  Google Scholar 

  10. National Cancer Institute D, Surveillance Research Program, Surveillance Systems Branch: Surveillance, Epidemiology, and End Results (SEER) Program Populations (1969–2014) In

  11. Rutherford MJ, Lambert PC, Thompson JR (2010) Age-period-cohort modeling. Stata J 10:606–627

    Google Scholar 

  12. Carstensen B (2007) Age-period-cohort models for the Lexis diagram. Stat Med 26:3018–3045

    Article  CAS  PubMed  Google Scholar 

  13. McGlynn KA, Tarone RE, El-Serag HB (2006) A comparison of trends in the incidence of hepatocellular carcinoma and intrahepatic cholangiocarcinoma in the United States. Cancer Epidemiol Biomarkers Prev 15:1198–1203

    Article  PubMed  Google Scholar 

  14. Etxeberria J, Goicoa T, López-Abente G et al (2017) Spatial gender-age-period-cohort analysis of pancreatic cancer mortality in Spain (1990–2013). PLoS One 12:e0169751

    Article  PubMed  PubMed Central  Google Scholar 

  15. Gao X, Wang Z, Kong C, Yang F, Wang Y, Tan X (2017) Trends of esophageal cancer mortality in rural China from 1989 to 2013: an age-period-cohort analysis. Int J Environ Res Public Health. doi:10.3390/ijerph14030218

    Google Scholar 

  16. Liang D, Liang S, Jin J et al (2017) Gastric cancer burden of last 40 years in North China (Hebei Province): a population-based study. Medicine (Baltimore) 96:e5887

    Article  Google Scholar 

  17. Arbeev KG, Ukraintseva SV, Arbeeva LS, Yashin AI (2005) Decline in human cancer incidence rates at old ages: age-period-cohort considerations. Demogr Res 12:273–300

    Article  Google Scholar 

  18. Robinson WR, Utz RL, Keyes KM et al (2013) Birth cohort effects on abdominal obesity in the United States: the Silent Generation, Baby Boomers and Generation X. Int J Obes (Lond) 37:1129–1134

    Article  CAS  Google Scholar 

  19. Njei B, Rotman Y, Ditah I, Lim JK (2015) Emerging trends in hepatocellular carcinoma incidence and mortality. Hepatology 61:191–199

    Article  PubMed  Google Scholar 

  20. Baumert TF, Jühling F, Ono A, Hoshida Y (2017) Hepatitis C-related hepatocellular carcinoma in the era of new generation antivirals. BMC Med 15:52

    Article  PubMed  PubMed Central  Google Scholar 

  21. Denniston MM, Klevens RM, McQuillan GM, Jiles RB (2012) Awareness of infection, knowledge of hepatitis C, and medical follow-up among individuals testing positive for hepatitis C: National Health and Nutrition Examination Survey 2001–2008. Hepatology 55:1652–1661

    Article  PubMed  PubMed Central  Google Scholar 

  22. Edlin BR (2016) Access to treatment for hepatitis C virus infection: time to put patients first. Lancet Infect Dis 16:e196–e201

    Article  PubMed  Google Scholar 

  23. Ogden CL, Carroll MD, Lawman HG et al (2016) Trends in obesity prevalence among children and adolescents in the United States, 1988–1994 through 2013–2014. JAMA 315:2292–2299

    Article  CAS  PubMed  Google Scholar 

  24. Schwimmer JB, Deutsch R, Kahen T et al (2006) Prevalence of fatty liver in children and adolescents. Pediatrics 118:1388–1393

    Article  PubMed  Google Scholar 

  25. Rashid M, Roberts EA (2000) Nonalcoholic steatohepatitis in children. J Pediatr Gastroenterol Nutr 30:48–53

    Article  CAS  PubMed  Google Scholar 

  26. Younossi Z, Henry L (2016) Contribution of alcoholic and nonalcoholic fatty liver disease to the burden of liver-related morbidity and mortality. Gastroenterology 150:1778–1785

    Article  PubMed  Google Scholar 

  27. Menahem B, Lubrano J, Duvoux C, Mulliri A, Alves A, Costentin C, Mallat A, Launoy G, Laurent A (2017) Liver transplantation versus liver resection for hepatocellular carcinoma in intention to treat: an attempt to perform an ideal meta-analysis. Liver Transpl 23(6):836–844. doi:10.1002/lt.24758

    Article  PubMed  Google Scholar 

  28. Murali AR, Patil S, Phillips KT, Voigt M (2017) Locoregional therapy with curative intent versus primary liver transplant for hepatocellular carcinoma: systematic review and meta-analysis. Transplantation 101:e249–e257

    Article  PubMed  Google Scholar 

  29. Yu JB, Gross CP, Wilson LD, Smith BD (2009) NCI SEER public-use data: applications and limitations in oncology research. Oncology (Williston Park) 23:288–295

    Google Scholar 

  30. White DL, Thrift AP, Kanwal F et al (2017) Incidence of hepatocellular carcinoma in all 50 United States, from 2000 through 2012. Gastroenterology 152:812–820

    Article  PubMed  Google Scholar 

  31. Lortet-Tieulent J, Soerjomataram I, Lin CC, Coebergh JW, Jemal A (2016) U.S. burden of cancer by race and ethnicity according to disability-adjusted life years. Am J Prev Med 51(5):673–681. doi:10.1016/j.amepre.2016.07.039

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Surgical Oncology, Department of Surgery, The Ohio State University Wexner Medical Center, James Cancer Hospital and Solove Research Institute, 395 W. 12th Ave., Suite 670, Columbus, OH, USA

    Eliza W. Beal, Ali Kabir, Dimitrios Moris, Xu-Feng Zhang, Jeffery Chakedis, Carl M. Schmidt & Timothy M. Pawlik

  2. Department of Anesthesiology and Pain Medicine, Nationwide Children’s Hospital, Columbus, OH, USA

    Dmitry Tumin

  3. Division of Transplant, Department of Surgery, The Ohio State University Wexner Medical Center, Columbus, OH, USA

    Kenneth Washburn & Sylvester Black

  4. Department of Hepatobiliary Surgery and Institute of Advanced Surgical Technology and Engineering, The First Affiliated Hospital of Xi’an Jiaotong University, Xi’an, China

    Xu-Feng Zhang

  5. Minimally Invasive Surgery Research Center, Iran University of Medical Sciences, Tehran, Iran

    Ali Kabir

Authors
  1. Eliza W. Beal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dmitry Tumin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ali Kabir
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dimitrios Moris
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xu-Feng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jeffery Chakedis
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Kenneth Washburn
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Sylvester Black
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Carl M. Schmidt
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Timothy M. Pawlik
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

EWB, DT, AK, DM, XZ, JC, KW, SMB, CRS, and TMP designed the study. EWB and DT performed the data analysis. EWB, DT, AK, DM, XZ, JC, KW, SMB, CRS, and TMP interpreted the data. EWB and DT prepared the manuscript. EWB, DT, AK, DM, XZ, JC, KW, SMB, CRS, and TMP provided critical review and approved the final version of the manuscript.

Corresponding author

Correspondence to Timothy M. Pawlik.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Beal, E.W., Tumin, D., Kabir, A. et al. Cohort Contributions to Race- and Gender-Specific Trends in the Incidence of Hepatocellular Carcinoma in the USA. World J Surg 42, 835–840 (2018). https://doi.org/10.1007/s00268-017-4194-1

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00268-017-4194-1

Search

Navigation