Incidence of primary liver cancer in American Indians and Alaska Natives, US, 1999–2009

Abstract

Purpose

To evaluate liver cancer incidence rates and risk factor correlations in non-Hispanic AI/AN populations for the years 1999–2009.

Methods

We linked data from 51 central cancer registries with the Indian Health Service patient registration databases to improve identification of the AI/AN population. Analyses were restricted to non-Hispanic persons living in Contract Health Service Delivery Area counties. We compared age-adjusted liver cancer incidence rates (per 100,000) for AI/AN to white populations using rate ratios. Annual percent changes (APCs) and trends were estimated using joinpoint regression analyses. We evaluated correlations between regional liver cancer incidence rates and risk factors using Pearson correlation coefficients.

Results

AI/AN persons had higher liver cancer incidence rates than whites overall (11.5 versus 4.8, RR = 2.4, 95% CI 2.3–2.6). Rate ratios ranged from 1.6 (Southwest) to 3.4 (Northern Plains and Alaska). We observed an increasing trend among AI/AN persons (APC 1999–2009 = 5%). Rates of distant disease were higher in the AI/AN versus white population for all regions except Alaska. Alcohol use (r = 0.84) and obesity (r = 0.79) were correlated with liver cancer incidence by region.

Conclusions

Findings highlight disparities in liver cancer incidence between AI/AN and white populations and emphasize opportunities to decrease liver cancer risk factor prevalence.

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Fig. 1

References

  1. 1.

    Ryerson AB, Eheman CR, Altekruse SF et al (2016) Annual Report to the Nation on the Status of Cancer, 1975–2012, featuring the increasing incidence of liver cancer. Cancer 122:1312–1337

    Article  PubMed  PubMed Central  Google Scholar 

  2. 2.

    Jim MA, Perdue DG, Richardson LC et al (2008) Primary liver cancer incidence among American Indians and Alaska Natives, US, 1999–2004. Cancer 113:1244–1255

    Article  PubMed  Google Scholar 

  3. 3.

    White MC, Espey DK, Swan J, Wiggins CL, Eheman C, Kaur JS (2014) Disparities in cancer mortality and incidence among American Indians and Alaska Natives in the United States. Am J Public Health 104(Suppl 3):S377–S387

    Article  PubMed  PubMed Central  Google Scholar 

  4. 4.

    Di Bisceglie AM, Lyra AC, Schwartz M et al (2003) Hepatitis C-related hepatocellular carcinoma in the United States: influence of ethnic status. Am J Gastroenterol 98:2060–2063

    PubMed  Google Scholar 

  5. 5.

    Armstrong GL, Wasley A, Simard EP, McQuillan GM, Kuhnert WL, Alter MJ (2006) The prevalence of hepatitis C virus infection in the United States, 1999 through 2002. Ann Intern Med 144:705–714

    Article  PubMed  Google Scholar 

  6. 6.

    Perz JF, Armstrong GL, Farrington LA, Hutin YJ, Bell BP (2006) The contributions of hepatitis B virus and hepatitis C virus infections to cirrhosis and primary liver cancer worldwide. J Hepatol 45:529–538

    Article  PubMed  Google Scholar 

  7. 7.

    Marrero JA, Fontana RJ, Fu S, Conjeevaram HS, Su GL, Lok AS (2005) Alcohol, tobacco and obesity are synergistic risk factors for hepatocellular carcinoma. J Hepatol 42:218–224

    Article  PubMed  CAS  Google Scholar 

  8. 8.

    Espey DK, Wiggins CL, Jim MA, Miller BA, Johnson CJ, Becker TM (2008) Methods for improving cancer surveillance data in American Indian and Alaska Native populations. Cancer 113:1120–1130

    Article  PubMed  Google Scholar 

  9. 9.

    Hankey BF, Ries LA, Edwards BK (1999) The surveillance, epidemiology, and end results program: a national resource. Cancer Epidemiol Biomarkers Prev 8:1117–1121

    PubMed  CAS  Google Scholar 

  10. 10.

    Thoburn KK, German RR, Lewis M, Nichols PJ, Ahmed F, Jackson-Thompson J (2007) Case completeness and data accuracy in the Centers for Disease Control and Prevention’s National Program of Cancer Registries. Cancer 109:1607–1616

    Article  PubMed  Google Scholar 

  11. 11.

    Young JL, Roffers SD, Ries LAG, Fritz AG, Hurlbut AA (eds) (2001) SEER Summary Sating Manual-2000: Codes and Coding Instructions. NIH Publication No. 01-4969. National Cancer Institute, Bethesda

    Google Scholar 

  12. 12.

    National Center for Chronic Disease Prevention and Health Promotion (2005) Link Plus: A suite of publicly available software programs for collecting and processing cancer registry data. Atlanta Ga: Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, U.S. Department of Health and Human Services. http://www.cdc.gov/cancer/npcr/tools/registryplus/lp.htm. Accessed on 18 Oct 2016

  13. 13.

    U.S. Department of Health and Human Services (2017) Indian health service. Purchased/Referred Care. Contract Health Service Delivery Areas (CHSDA). https://www.ihs.gov/prc/index.cfm?module=chs_requirements_chsda. Accessed Nov 2017

  14. 14.

    Arias E, Schauman WS, Eschbach K, Sorlie PD, Backlund E (2008) The validity of race and Hispanic origin reporting on death certificates in the United States. Vital Health Stat 2:1–23

    Google Scholar 

  15. 15.

    Behavioral Risk Factor Surveillance System Survey Data. Atlanta, Georgia: U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, 1999–2009. https://www.cdc.gov/brfss/annual_data/

  16. 16.

    National Cancer Institute. Surveillance, Epidemiology, and End Results (SEER) Program. Statistical Resources. U.S. population data 1969–2011. http://seer.cancer.gov/popdata/. Accessed on 10 June 2013

  17. 17.

    Jim MA, Arias E, Seneca DS et al (2014) Racial misclassification of American Indians and Alaska Natives by Indian health service contract health service delivery area. Am J Public Health 104(Suppl 3):S295–S302

    Article  PubMed  PubMed Central  Google Scholar 

  18. 18.

    Surveillance Research Program, National Cancer Institute. SEER*Stat Software, Latest Release: 8.3.2 (2016) http://seer.cancer.gov/seerstat. Accessed Oct 2016

  19. 19.

    Kim HJ, Fay MP, Feuer EJ, Midthune DN (2000) Permutation tests for joinpoint regression with applications to cancer rates. Stat Med 19:335–351

    Article  PubMed  CAS  Google Scholar 

  20. 20.

    National Cancer Institute. Joinpoint regression program, Version 4.3.1.0 (2016) Bethesda, MD: National Cancer Institute. http://surveillance.cancer.gov/joinpoint. Accessed 15 Nov 2016

  21. 21.

    Tiwari RC, Clegg LX, Zou Z (2006) Efficient interval estimation for age-adjusted cancer rates. Stat Methods Med Res 15:547–569

    Article  PubMed  Google Scholar 

  22. 22.

    de Martel C, Maucort-Boulch D, Plummer M, Franceschi S (2015) World-wide relative contribution of hepatitis B and C viruses in hepatocellular carcinoma. Hepatology 62:1190–1200

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. 23.

    Reilley B, Leston J, Hariri S et al (2016) Birth cohort testing for hepatitis C virus - Indian health service 2012–2015. MMWR Morb Mortal Wkly Rep 65:467–469

    Article  PubMed  Google Scholar 

  24. 24.

    Leston J, Finkbonner J (2016) The need to expand access to hepatitis C virus drugs in the Indian Health Service. JAMA 316:817–818

    Article  PubMed  Google Scholar 

  25. 25.

    McMahon BJ, Bulkow LR, Singleton RJ et al (2011) Elimination of hepatocellular carcinoma and acute hepatitis B in children 25 years after a hepatitis B newborn and catch-up immunization program. Hepatology 54:801–807

    Article  PubMed  Google Scholar 

  26. 26.

    Connelly M, Bruce MG, Bulkow L, Snowball M, McMahon BJ (2016) The changing epidemiology and aetiology of hepatocellular carcinoma from 1969 through 2013 in Alaska Native people. Liver Int 36:1829–1835

    Article  PubMed  CAS  Google Scholar 

  27. 27.

    Welzel TM, Graubard BI, Quraishi S et al (2013) Population-attributable fractions of risk factors for hepatocellular carcinoma in the United States. Am J Gastroenterol 108:1314–1321

    Article  PubMed  PubMed Central  Google Scholar 

  28. 28.

    CDC Chronic Disease Prevention and Health Promotion, Tribal Resources. Atlanta, Georgia: U.S Department of Health and Human Services, Centers for Disease Control and Prevention https://www.cdc.gov/chronicdisease/tribal/factsheet.htm. Accessed Feb 2017

  29. 29.

    Cobb N, Espey D, King J (2014) Health behaviors and risk factors among American Indians and Alaska Natives, 2000–2010. Am J Public Health 104(Suppl 3):S481–S489

    Article  PubMed  PubMed Central  Google Scholar 

  30. 30.

    Larsson SC, Wolk A (2007) Overweight, obesity and risk of liver cancer: a meta-analysis of cohort studies. Br J Cancer 97:1005–1008

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. 31.

    Neuschwander-Tetri BA, Caldwell SH (2003) Nonalcoholic steatohepatitis: summary of an AASLD Single Topic Conference. Hepatology 37:1202–1219

    Article  PubMed  Google Scholar 

  32. 32.

    Connolly GC, Safadjou S, Chen R et al (2012) Diabetes mellitus is associated with the presence of metastatic spread at disease presentation in hepatocellular carcinoma. Cancer Invest 30:698–702

    Article  PubMed  Google Scholar 

  33. 33.

    White DL, Ratziu V, El-Serag HB (2008) Hepatitis C infection and risk of diabetes: a systematic review and meta-analysis. J Hepatol 49:831–844

    Article  PubMed  PubMed Central  Google Scholar 

  34. 34.

    Tanaka K, Hirohata T, Takeshita S et al (1992) Hepatitis B virus, cigarette smoking and alcohol consumption in the development of hepatocellular carcinoma: a case–control study in Fukuoka, Japan. Int J Cancer 51:509–514

    Article  PubMed  CAS  Google Scholar 

  35. 35.

    Yuan JM, Govindarajan S, Arakawa K, Yu MC (2004) Synergism of alcohol, diabetes, and viral hepatitis on the risk of hepatocellular carcinoma in blacks and whites in the U.S. Cancer 101:1009–1017

    Article  PubMed  Google Scholar 

  36. 36.

    Landen M, Roeber J, Naimi T, Nielsen L, Sewell M (2014) Alcohol-attributable mortality among American Indians and Alaska Natives in the United States, 1999–2009. Am J Public Health 104(Suppl 3):S343–S349

    Article  PubMed  PubMed Central  Google Scholar 

  37. 37.

    Arora S, Thornton K, Murata G et al (2011) Outcomes of treatment for hepatitis C virus infection by primary care providers. N Engl J Med 364:2199–2207

    Article  PubMed  CAS  Google Scholar 

  38. 38.

    Arora S, Kalishman S, Thornton K et al (2016) Project ECHO (project extension for community healthcare outcomes): a national and global model for continuing professional development. J Contin Educ Health Prof 36(Suppl 1):S48–S49

    Article  PubMed  Google Scholar 

  39. 39.

    Recommendations for prevention and control of hepatitis C virus (HCV) infection and HCV-related chronic disease (1998) Centers for disease control and prevention. MMWR Recomm Rep 47:1–39

    Google Scholar 

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Acknowledgments

This study was supported by the Centers for Disease Control and Prevention (CDC). We thank Brian McMahon, Brenna Simons-Petrusa, and Sarah H. Nash from the Alaska Native Tribal Health Consortium for their input in this article.

Disclaimer

The findings and conclusions in this report are those of the authors and do not necessarily reflect the official position of the Centers for Disease Control and Prevention.

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Correspondence to Stephanie C. Melkonian.

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No conflicts of interest to disclose.

Ethical approval

The study did not involve human participants, institutional review board approval was not necessary.

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Melkonian, S.C., Jim, M.A., Reilley, B. et al. Incidence of primary liver cancer in American Indians and Alaska Natives, US, 1999–2009. Cancer Causes Control 29, 833–844 (2018). https://doi.org/10.1007/s10552-018-1059-3

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Keywords

  • Cancer incidence
  • American Indian
  • Alaska Native
  • Liver cancer
  • Health disparity