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Geographic epidemiology of hepatocellular carcinoma, viral hepatitis, and socioeconomic position in New York City

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Abstract

Purpose

Liver cancer (hepatocellular carcinoma (HCC)) incidence and mortality rates are increasing in the United States. New York City (NYC) has a high burden of liver cancer risk factors, including hepatitis C (HCV) and hepatitis B (HBV) infection, which disproportionately affect persons of low socioeconomic position. Identifying neighborhoods with HCC disparities is essential to effectively define targeted cancer control strategies.

Methods

New York State Cancer Registry data from 1 January 2001 through 31 December 2012 were matched with NYC HCV and HBV surveillance data. HCC data were aggregated to NYC Zip Code Tabulation Areas (ZCTAs). Moran’s I cluster analysis, Poisson regression, and geographically weighted Poisson regression were used to identify hotspots in HCC incidence and to examine the spatial associations with viral hepatitis rates, poverty, and uninsured status.

Results

Among NYC residents, 8,827 HCC cases were diagnosed during 2001–2012. Significant clustering was detected in the HCC rates (Moran’s I = 0.25) with the strongest clustering found in HCC patients with comorbid HCV infection (Moran’s I = 0.47). Poverty and uninsured status were associated (p < 0.05) with increased rates of HCC patients with HBV or HCV infection. Neighborhoods with high rates of HCC without viral hepatitis infection had lower rates of poverty and uninsured status.

Conclusions

The geographic variation in HCC highlights the need for neighborhood-targeted interventions to address risk factors and barriers to care. The clusters of HCC by viral hepatitis status may serve as a basis for healthcare policymakers and practitioners to prioritize neighborhoods for cancer screening and control efforts.

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Abbreviations

HCC:

Hepatocellular carcinoma

HCV:

Hepatitis C

HBV:

Hepatitis B

AIC:

Akaike information criterion

BIC:

Bayesian information criteria

GWPR:

Geographically weighted Poisson regression

LISA:

Local indicators of spatial autocorrelation

ZCTA:

Zip Code Tabulation Area

References

  1. Surveillance, Epidemiology, and End Results (SEER) Program (http://www.seer.cancer.gov) Research Data (1973–2011) (2014 based on the Nov 2013 submission). National Cancer Institute DCCPS Surveillance Research Program, Surveillance Systems Branch

  2. Cancer incidence and mortality by year, New York City 1976–2013 (2015). New York State Cancer Registry

  3. Surveillance, Epidemiology, and End Results (SEER) Program (http://www.seer.cancer.gov) SEER*Stat Database. SEER 18 Regs Research Data + Hurricane Katrina impacted Louisiana cases, Nov 2014 Sub (1973–2012 varying)—linked to county attributes—total U.S., 1969–2013 counties, (2015, based on November 2014 submission)

  4. El-Serag HB (2007) Epidemiology of hepatocellular carcinoma in USA. Hepatol Res 37(Suppl 2):S88–S94. doi:10.1111/j.1872-034X.2007.00168.x

    Article  PubMed  Google Scholar 

  5. El-Serag HB (2011) Hepatocellular carcinoma. N Engl J Med 365(12):1118–1127. doi:10.1056/NEJMra1001683

    Article  CAS  PubMed  Google Scholar 

  6. El-Serag HB (2012) Epidemiology of viral hepatitis and hepatocellular carcinoma. Gastroenterology 142(6):1264–1273. doi:10.1053/j.gastro.2011.12.061 e1261

    Article  PubMed  PubMed Central  Google Scholar 

  7. Hepatitis B and C Surveillance Report, 2013 (2013) New York City Department of Health & Mental Hygeine, New York

  8. Siminoff LA, Ross L (2005) Access and equity to cancer care in the USA: a review and assessment. Postgrad Med J 81(961):674–679. doi:10.1136/pgmj.2005.032813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Poverty Data Tool (2012) Poverty research team. NYC Center for Economic Opportunity New York, New York

    Google Scholar 

  10. Ward E, Halpern M, Schrag N, Cokkinides V, DeSantis C, Bandi P, Siegel R, Stewart A, Jemal A (2008) Association of insurance with cancer care utilization and outcomes. CA Cancer J Clin 58(1):9–31. doi:10.3322/CA.2007.0011

    Article  PubMed  Google Scholar 

  11. El-Serag HB, Rudolph KL (2007) Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 132(7):2557–2576. doi:10.1053/j.gastro.2007.04.061

    Article  CAS  PubMed  Google Scholar 

  12. Shebl FM, Capo-Ramos DE, Graubard BI, McGlynn KA, Altekruse SF (2012) Socioeconomic status and hepatocellular carcinoma in the United States. Cancer Epidemiol Biomark Prev 21(8):1330–1335. doi:10.1158/1055-9965.EPI-12-0124

    Article  Google Scholar 

  13. Major JM, Sargent JD, Graubard BI, Carlos HA, Hollenbeck AR, Altekruse SF, Freedman ND, McGlynn KA (2014) Local geographic variation in chronic liver disease and hepatocellular carcinoma: contributions of socioeconomic deprivation, alcohol retail outlets, and lifestyle. Ann Epidemiol 24(2):104–110. doi:10.1016/j.annepidem.2013.11.006

    Article  PubMed  Google Scholar 

  14. Shepard CW, Finelli L, Alter MJ (2005) Global epidemiology of hepatitis C virus infection. Lancet Infect Dis 5(9):558–567. doi:10.1016/S1473-3099(05)70216-4

    Article  PubMed  Google Scholar 

  15. Kaplan GA (1996) People and places: contrasting perspectives on the association between social class and health. Int J Health Serv 26(3):507–519

    Article  CAS  PubMed  Google Scholar 

  16. Yen IH, Kaplan GA (1999) Neighborhood social environment and risk of death: multilevel evidence from the Alameda County Study. Am J Epidemiol 149(10):898–907

    Article  CAS  PubMed  Google Scholar 

  17. Ten U.S. cities now have 1 million people or more; California and Texas each have three of these places (2015) News releases. United States Census Bureau

  18. Population Facts (2014) Department of City Planning New York, New York

  19. The Center for Economic Opportunity (CEO) Poverty Measure, 2005–2012. An Annual Report from the Office of the Mayor (2014). Poverty Research Team, NYC Center for Economic Opportunity New York, New York

  20. Geographic Terms and Concepts—Zip Code Tabulation Areas. (2012) United States Census Bureau. https://www.census.gov/geo/reference/gtc/gtc_zcta.html

  21. Braveman P, Gottlieb L (2014) The social determinants of health: it’s time to consider the causes of the causes. Public Health Rep 129(Suppl 2):19–31

    Article  PubMed  PubMed Central  Google Scholar 

  22. Anselin L, Syabri I, Kho Y (2006) GeoDa: an introduction to spatial data analysis. Geogr Anal 38(1):5–22

    Article  Google Scholar 

  23. Anselin L (2005) Exploring spatial data with GeoDa: a workbook. Center for Spatially Integrated Social Science. http://www.csiss.org/clearinghouse/GeoDa/geodaworkbook.pdf

  24. Huang X, Jensen C, Šaltenis S (2005) The islands approach to nearest neighbor querying in spatial networks. In: Medeiros CB, Egenhofer M, Bertino E (eds) Advances in spatial and temporal databases, vol 3633., Lecture notes in computer scienceSpringer, Berlin, pp 73–90. doi:10.1007/11535331_5

    Chapter  Google Scholar 

  25. Nakaya T, Fotheringham A, Brunsdon C, Charlton M (2005) Geographically weighted Poisson regression for disease association mapping. Stat Med 24(17):2695–2717

    Article  CAS  PubMed  Google Scholar 

  26. Matkan AA, Mohaymany AS, Mirbagheri B, Shahri M (2011) Explorative spatial analysis of traffic accidents using GWPR model for urban safety planning. In: 3rd International Conference on Road Safety and Simulation

  27. Nakaya T, Fotheringham AS, Brunsdon C, Charlton M (2005) Geographically weighted Poisson regression for disease association mapping. Stat Med 24(17):2695–2717. doi:10.1002/sim.2129

    Article  CAS  PubMed  Google Scholar 

  28. Weisent J, Rohrbach B, Dunn JR (2012) Socioeconomic determinants of geographic disparities in campylobacteriosis risk: a comparison of global and local modeling approaches. Int J Health Geogr 11(1):45

    Article  PubMed  PubMed Central  Google Scholar 

  29. Nakaya T, Charlton M, Lewis P, Brunsdon C, Yao J, Fotheringham AS (2009) GWR4 windows application for geographically weighted regression modelling. GWR 4 Development Team

  30. Hogrebe MC, Tate WF (2012) Place, poverty, and algebra: a statewide comparative spatial analysis of variable relationships. J Mathematics Educ Teach Coll 3(2):12–24

    Google Scholar 

  31. Yun EH, Lim MK, Oh JK, Park JH, Shin A, Sung J, Park EC (2010) Combined effect of socioeconomic status, viral hepatitis, and lifestyles on hepatocellular carcinoma risk in Korea. Br J Cancer 103(5):741–746. doi:10.1038/sj.bjc.6605803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Tohme RA, Xing J, Liao Y, Holmberg SD (2013) Hepatitis C testing, infection, and linkage to care among racial and ethnic minorities in the United States, 2009–2010. Am J Public Health 103(1):112–119. doi:10.2105/AJPH.2012.300858

    Article  PubMed  PubMed Central  Google Scholar 

  33. Stepanova M, Kanwal F, El-Serag HB, Younossi ZM (2011) Insurance status and treatment candidacy of hepatitis C patients: analysis of population-based data from the United States. Hepatology 53(3):737–745. doi:10.1002/hep.24131

    Article  PubMed  Google Scholar 

  34. Rodriguez-Torres M (2008) Latinos and chronic hepatitis C: a singular population. Clin Gastroenterol 6(5):484–490. doi:10.1016/j.cgh.2008.02.036

    Article  Google Scholar 

  35. Anyiwe K, Qiao Y, De P, Yoshida EM, Earle CC, Thein HH (2015) Effect of socioeconomic status on hepatocellular carcinoma incidence and stage at diagnosis, a population-based cohort study. Liver Int. doi:10.1111/liv.12982

    PubMed  Google Scholar 

  36. Halpern MT, Ward EM, Pavluck AL, Schrag NM, Bian J, Chen AY (2008) Association of insurance status and ethnicity with cancer stage at diagnosis for 12 cancer sites: a retrospective analysis. Lancet Oncol 9(3):222–231. doi:10.1016/S1470-2045(08)70032-9

    Article  PubMed  Google Scholar 

  37. Zaydfudim V, Whiteside MA, Griffin MR, Feurer ID, Wright JK, Pinson CW (2010) Health insurance status affects staging and influences treatment strategies in patients with hepatocellular carcinoma. Ann Surg Oncol 17(12):3104–3111. doi:10.1245/s10434-010-1181-2

    Article  PubMed  Google Scholar 

  38. Mitchell T, Armstrong GL, Hu DJ, Wasley A, Painter JA (2011) The increasing burden of imported chronic hepatitis B-United States, 1974–2008. PLoS One 6(12):e27717. doi:10.1371/journal.pone.0027717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Galea S, Ahern J, Tracy M, Vlahov D (2007) Neighborhood income and income distribution and the use of cigarettes, alcohol, and marijuana. Am J Prev Med 32(6 Suppl):S195–S202. doi:10.1016/j.amepre.2007.04.003

    Article  PubMed  PubMed Central  Google Scholar 

  40. Yang JD, Harmsen WS, Slettedahl SW, Chaiteerakij R, Enders FT, Therneau TM, Orsini L, Kim WR, Roberts LR (2011) Factors that affect risk for hepatocellular carcinoma and effects of surveillance. Clin Gastroenterol Hepatol 9(7):617–623. doi:10.1016/j.cgh.2011.03.027 e611

    Article  PubMed  Google Scholar 

  41. Prevalence of current, heavy, and binge drinking (past 30 days) among adults by demographics, New York City, 2013. New York City Department of Health and Mental Hygeine

  42. Janelle DG, Warf, B., Hansen, K. (ed) (2004) WorldMinds: geographical perspectives on 100 problems. Commemorating the 100th anniversary of the Association of American Geographers 1904–2004 Springer, B.V

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Authors and Affiliations

  1. Division of Disease Control, Bureau of Communicable Disease, New York City Department of Health and Mental Hygiene, 42-09 28th St, Long Island City, NY, 11101, USA

    Mary M. Ford, Payal Desai & Fabienne Laraque

  2. Division of Epidemiology, New York City Department of Health and Mental Hygiene, 42-09 28th St, Long Island City, NY, 11101, USA

    Elena Ivanina

  3. Department of Management, Policy and Community Health Practice, University of Texas School of Public Health, 1200 Pressler RAS Bldg., E913, Houston, TX, 77030, USA

    Linda Highfield

  4. New York State Department of Health, Bureau of Cancer Epidemiology, 150 Broadway Suite 361, Albany, NY, 12204, USA

    Baozhen Qiao & Maria J. Schymura

Authors
  1. Mary M. Ford
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  2. Elena Ivanina
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  7. Fabienne Laraque
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Correspondence to Mary M. Ford.

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Ford, M.M., Ivanina, E., Desai, P. et al. Geographic epidemiology of hepatocellular carcinoma, viral hepatitis, and socioeconomic position in New York City. Cancer Causes Control 28, 779–789 (2017). https://doi.org/10.1007/s10552-017-0897-8

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  • DOI: https://doi.org/10.1007/s10552-017-0897-8

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