Skip to main content
SpringerLink
Log in

Medical history and the risk of biliary tract cancers in Shanghai, China: implications for a role of inflammation

  • Original paper
  • Published:
Cancer Causes & Control Aims and scope Submit manuscript

Abstract

Several lines of evidence suggest that inflammation may play a role in the etiology of biliary tract cancers. To examine further the role of inflammation, we evaluated the associations between self-reported inflammatory-related medical conditions and the risk of biliary tract cancers in a population-based case–control study in Shanghai, China. Our analysis included 368 gallbladder cancer cases, 191 bile duct cancer cases, 68 ampulla of Vater cancer cases, and 959 healthy subjects. We used logistic regression to estimate odds ratios (ORs) and 95% confidence intervals (CIs) for biliary tract cancers in relation to six inflammation-related conditions. Gallbladder cancer was significantly associated with cholecystitis occurring at least 5 years prior to interview (OR = 1.7, 95% CI 1.1–2.9). Even though biliary stones did not significantly modify the associations between cholecystitis and gallbladder cancer, 90% of the gallbladder cancer cases with cholecystitis also had biliary stones, indicating that stones likely play an important role in the link between cholecystitis and gallbladder cancer. Among subjects who smoked and drank alcohol, a history of gastric (OR = 4.3, 95% CI 1.2–15.0) or duodenal ulcers (OR = 3.7, 1.2–12.0) was associated with an excess risk of gallbladder cancer. Although the mechanisms are unclear, our results further support the role for inflammation in the etiology of biliary tract cancers.

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

Similar content being viewed by others

References

  1. Hsing AW, Rashid A, Devesa SS, Fraumeni JF Jr (2006) Biliary tract cancer. In: Schottenfeld D, Fraumeni JF Jr (eds) Cancer epidemiology and prevention, 3rd edn. Oxford University Press, Oxford, pp 787–800

    Chapter  Google Scholar 

  2. Portincasa P, van de Meeberg P, van Erpecum KJ, Palasciano G, VanBerge-Henegouwen GP (1997) An update on the pathogenesis and treatment of cholesterol gallstones. Scand J Gastroenterol Suppl 223:60–69

    PubMed  CAS  Google Scholar 

  3. Hsing AW, Rashid A, Sakoda LC, Deng J, Han TQ, Wang BS, Shen MC, Fraumeni JF Jr, Gao YT (2007) Gallstones and the risk of biliary tract cancer: a population-based study. Br J Cancer 97:1577–1582

    Article  PubMed  CAS  Google Scholar 

  4. Grimble RF (2002) Inflammatory status and insulin resistance. Curr Opin Clin Nutr Metab Care 5:551–559

    Article  PubMed  CAS  Google Scholar 

  5. Marette A (2002) Mediators of cytokine-induced insulin resistance in obesity and other inflammatory settings. Curr Opin Clin Nutr Metab Care 5:377–383

    Article  PubMed  CAS  Google Scholar 

  6. Hsing AW, Sakoda LC, Rashid A, Chen J, Shen MC, Han TQ, Wang BS, Gao YT (2008) Body size and the risk of biliary tract cancer: a population-based study in China. Br J Cancer 99:811–815

    Article  PubMed  CAS  Google Scholar 

  7. Andreotti G, Chen J, Gao YT, Rashid A, Chang SC, Shen MC, Wang BS, Han TQ, Zhang BH, Danforth KN, Althuis MD, Hsing AW (2008) Serum lipid levels and the risk of biliary tract cancers and biliary stones: a population-based study in China. Int J Cancer 122:2322–2329

    Article  PubMed  CAS  Google Scholar 

  8. Shebl FM, Andreotti G, Rashid A, Gao YT, Yu K, Shen MC, Wang BS, Wang BS, Li Q, Han TQ, Zhang BH, Fraumeni JF, Hsing AW. Biliary tract cancer and stones in relation to diabetes mellitus: a population based study in Shanghai, China. Br J Cancer (accepted)

  9. Sheb FM, Andreotti G, Meyer TE, Gao YT, Rashid A, Yu K, Shen MC, Wang BS, Han TQ, Zhang BH, Stanczyk FZ, Fraumeni JF, Hsing AW. Metabolic syndrome and insulin resistance in relation to biliary tract cancer and stone risks: a population based study in Shanghai, China (submitted)

  10. Fox JG (1998) Review article: Helicobacter species and in vivo models of gastrointestinal cancer. Aliment Pharmacol Ther 1:37–60

    Article  Google Scholar 

  11. Sripa B, Kaewkes S, Sithithaworn P, Mairiang E, Laha T, Smout M, Pairojkul C, Bhudhisawasdi V, Tesana S, Thinkamrop B, Bethony JM, Loukas A, Brindley PJ (2007) Liver fluke induces cholangiocarcinoma. PLoS Med 4:e201

    Article  PubMed  Google Scholar 

  12. Hsing AW, Zhang M, Rashid A, McGlynn KA, Wang BS, Niwa S, Ortiz-Conde BA, Goedert JJ, Fraumeni JF Jr, O’Brien TR, Gao YT (2008) Hepatitis B and C virus infection and the risk of biliary tract cancer: a population-based study in China. Int J Cancer 122:1849–1853

    Article  PubMed  CAS  Google Scholar 

  13. Yanagisawa N, Mikami T, Koike M, Okayasu I (2000) Enhanced cell kinetics, p53 accumulation and high p21WAF1 expression in chronic cholecystitis: comparison with background mucosa of gallbladder carcinomas. Histopathology 36:54–61

    Article  PubMed  CAS  Google Scholar 

  14. Yanagisawa N, Mikami T, Yamashita K, Okayasu I (2003) Microsatellite instability in chronic cholecystitis is indicative of an early stage in gallbladder carcinogenesis. Am J Clin Pathol 120:413–416

    Article  PubMed  CAS  Google Scholar 

  15. Burak K, Angulo P, Pasha TM, Egan K, Petz J, Lindor KD (2004) Incidence and risk factors for cholangiocarcinoma in primary sclerosing cholangitis. Am J Gastroenterol 99:523–526

    Article  PubMed  Google Scholar 

  16. Nguyen T, Brunson D, Crespi CL, Penman BW, Wishnok JS, Tannenbaum SR (1992) DNA damage and mutation in human cells exposed to nitric oxide in vitro. Proc Natl Acad Sci USA 89:3030–3034

    Article  PubMed  CAS  Google Scholar 

  17. Ohshima H, Bartsch H (1994) Chronic infections and inflammatory processes as cancer risk factors: possible role of nitric oxide in carcinogenesis. Mutat Res 305:253–264

    PubMed  CAS  Google Scholar 

  18. Tazuma S, Kajiyama G (2001) Carcinogenesis of malignant lesions of the gall bladder. The impact of chronic inflammation and gallstones. Langenbecks Arch Surg 386:224–229

    Article  PubMed  CAS  Google Scholar 

  19. Schirmer BD, Winters KL, Edlich RF (2005) Cholelithiasis and cholecystitis. J Long Term Eff Med Implants 15:329–338

    Article  PubMed  Google Scholar 

  20. Albores-Saavedra J, de Jesus Manrique J, Angeles–Angeles A, Henson DE (1984) Carcinoma in situ of the gallbladder. A clinicopathologic study of 18 cases. Am J Surg Pathol 8:323–333

    Article  PubMed  CAS  Google Scholar 

  21. Kanoh K, Shimura T, Tsutsumi S, Suzuki H, Kashiwabara K, Nakajima T, Kuwano H (2001) Significance of contracted cholecystitis lesions as high risk for gallbladder carcinogenesis. Cancer Lett 169:7–14

    Article  PubMed  CAS  Google Scholar 

  22. Kawabe T, Isobe KI, Hasegawa Y, Nakashima I, Shimokata K (1992) Immunosuppressive activity induced by nitric oxide in culture supernatant of activated rat alveolar macrophages. Immunology 76:72–78

    PubMed  CAS  Google Scholar 

  23. Wee A, The M, Raju GC (1994) Clinical importance of p53 protein in gallbladder carcinoma and its precursor lesions. J Clin Pathol 47:453–456

    Article  PubMed  CAS  Google Scholar 

  24. Wistuba I, Sugio K, Hung J et al (1995) Allele-specific mutations involved in the pathogenesis of endemic gallbladder cancer in Chile. Cancer Res 55:2511–2515

    PubMed  CAS  Google Scholar 

  25. Hsing AW, Sakoda LC, Rashid A, Andreotti G, Chen J, Wang BS, Shen MC, Chen BE, Rosenberg PS, Zhang M, Niwa S, Chu L, Welch R, Yeager M, Fraumeni JF Jr, Gao YT, Chanock SJ (2008) Variants in inflammation genes and the risk of biliary tract cancers and stones: a population-based study in China. Cancer Res 68:6442–6452

    Article  PubMed  CAS  Google Scholar 

  26. Parasher G, Eastwood GL (2000) Smoking and peptic ulcer in the Helicobacter pylori era. Eur J Gastroenterol Hepatol 12:843–853

    Article  PubMed  CAS  Google Scholar 

  27. Franke A, Teyssen S, Singer MV (2005) Alcohol-related diseases of the esophagus and stomach. Dig Dis 23:204–213

    Article  PubMed  Google Scholar 

  28. Shimoyama T, Everett SM, Fukuda S, Axon AT, Dixon MF, Crabtree JE (2001) Influence of smoking and alcohol on gastric chemokine mRNA expression in patients with Helicobacter pylori infection. J Clin Pathol 54:332–334

    Article  PubMed  CAS  Google Scholar 

  29. Zatonski WA, Lowenfels AB, Boyle P, Maisonneuve P, de Mesquita HBB, Ghadirian P, Jain M, Przewozniak K, Baghurst P, Moerman CJ, Simard A, Howe GR, McMichael AJ, Hsieh CC, Walker AM (1997) Epidemiologic aspects of gallbladder cancer: a case–control study of the SEARCH program of the international agency for research on cancer. J Natl Cancer Inst 89:1132–1138

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank the collaborating surgeons and pathologists in Shanghai for assistance in patient recruitment and pathology review; Chia–Rong Cheng, Lu Sun, and Kai Wu of the Shanghai Cancer Institute for coordinating data and specimen collection; and Shelley Niwa of Westat for support with study and data management. The study was funded by the Intramural Research Program of the National Institute of Health, National Cancer Institute, Division of Cancer Epidemiology and Genetics, USA.

Author information

Authors and Affiliations

  1. Division of Cancer Epidemiology and Genetics, National Cancer Institute, 6120 Executive Blvd., EPS 8011, MSC 7240, Bethesda, MD, 20892, USA

    Gabriella Andreotti, Mahboobeh Safaeian & Ann W. Hsing

  2. Department of Epidemiology, Shanghai Cancer Institute, Shanghai, China

    Enju Liu, Yu-Tang Gao & Jie Deng

  3. Department of Pathology, MD Anderson Cancer Center, Houston, TX, USA

    Asif Rashid

  4. Shanghai Tumor Hospital, Fudan University, Shanghai, China

    Ming-Chang Shen

  5. Zhong Shan Hospital, Fudan University, Shanghai, China

    Bin-Shen Wang

  6. Department of Surgery, Rui Jin Hospital, Shanghai Second Medical University, Shanghai, China

    Tian-Quian Han

  7. Institute of East Hepatobiliary Surgery, Shanghai Second Military University, Shanghai, China

    Bai-He Zhang

Authors
  1. Gabriella Andreotti
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Enju Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yu-Tang Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mahboobeh Safaeian
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Asif Rashid
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ming-Chang Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Bin-Shen Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jie Deng
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Tian-Quian Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Bai-He Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Ann W. Hsing
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gabriella Andreotti.

Electronic supplementary material

Below is the link to the electronic supplementary material.

(PDF 65 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Andreotti, G., Liu, E., Gao, YT. et al. Medical history and the risk of biliary tract cancers in Shanghai, China: implications for a role of inflammation. Cancer Causes Control 22, 1289–1296 (2011). https://doi.org/10.1007/s10552-011-9802-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10552-011-9802-z

Keywords

Search

Navigation