Skip to main content
Log in

A meta-analysis of the clinicopathological characteristics and survival outcomes of inflammatory bowel disease associated colorectal cancer

  • Review
  • Published:
International Journal of Colorectal Disease Aims and scope Submit manuscript

Abstract

Purpose

The current study aims to use meta-analytical techniques to compare the clinicopathological characteristics and survival outcomes of inflammatory bowel disease (IBD) associated and sporadic colorectal carcinoma (CRC). Patients with IBD have an established increased risk of developing CRC. There is no consensus, however, on the clinicopathological characteristics and survival outcomes of IBD associated CRC when compared to sporadic CRC.

Methods

A comprehensive search for published studies comparing IBD associated and sporadic CRC was performed. Random effect methods were used to combine data. This study adhered to the recommendations of the MOOSE guidelines.

Results

Data were retrieved from 20 studies describing 571,278 patients. IBD associated CRC had an increased rate of synchronous tumors (OR 4.403, 95% CI 2.320–8.359; p < 0.001), poor differentiation (OR 1.875, 95% CI 1.425–2.466; p < 0.001), and a reduced rate of rectal cancer (OR 0.827, 95% CI 0.735–0.930; p = 0.002). IBD associated CRC however did not affect the frequency of T3/T4 tumors (OR 0.931, 95% CI 0.782–1.108; p = 0.421), lymph node positivity (OR 1.061, 95% CI 0.929–1.213; p = 0.381), metastasis at presentation (OR 0.970, 95% CI 0.776–1.211; p = 0.786), sex distribution (OR 0.978, 95% CI 0.890–1.074; p = 0.640), or 5-year overall survival (OR 1.105, 95% CI 0.414–2.949; p = 0.842).

Conclusions

In this large analysis of available data, IBD associated CRC was characterized by less rectal tumors and more synchronous and poorly differentiated tumors compared with sporadic cancers, but no discernable difference in sex distribution, stage at presentation, or survival could be identified.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Eaden JA, Abrams KR, Mayberry JF (2001) The risk of colorectal cancer in ulcerative colitis: a meta-analysis. Gut 48(4):526–535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Jess T, Rungoe C, Peyrin-Biroulet L (2012) Risk of colorectal cancer in patients with ulcerative colitis: a meta-analysis of population-based cohort studies. Clin Gastroenterol Hepatol 10(6):639–645

    Article  PubMed  Google Scholar 

  3. von Roon AC, Reese G, Teare J, Constantinides V, Darzi AW, Tekkis PP (2007) The risk of cancer in patients with Crohn’s disease. Dis Colon rectum 50(6):839–855

  4. Harpaz N, Peck AL, Yin J, Fiel I, Hontanosas M, Tong TR, Laurin JN, Abraham JM, Greenwald BD, Meltzer SJ (1994) p53 protein expression in ulcerative colitis-associated colorectal dysplasia and carcinoma. Hum Pathol 25(10):1069–1074

    Article  CAS  PubMed  Google Scholar 

  5. Burmer GC, Levine DS, Kulander BG, Haggitt RC, Rubin CE, Rabinovitch PS (1990) c-Ki-ras mutations in chronic ulcerative colitis and sporadic colon carcinoma. Gastroenterology 99(2):416–420

    Article  CAS  PubMed  Google Scholar 

  6. Garrity-Park MM, Loftus EV Jr, Bryant SC, Sandborn WJ, Smyrk TC (2008) Tumor necrosis factor-alpha polymorphisms in ulcerative colitis-associated colorectal cancer. Am J Gastroenterol 103(2):407–415

    Article  CAS  PubMed  Google Scholar 

  7. Larsen M, Mose H, Gislum M, Skriver MV, Jepsen P, Nørgård B, Sørensen HT (2007) Survival after colorectal cancer in patients with Crohn’s disease: a nationwide population-based Danish follow-up study. Am J Gastroenterol 102(1):163–167

    Article  PubMed  Google Scholar 

  8. Jensen AB, Larsen M, Gislum M, Skriver MV, Jepsen P, Nørgaard B, Sørensen HT (2006) Survival after colorectal cancer in patients with ulcerative colitis: a nationwide population-based Danish study. Am J Gastroenterol 101(6):1283–1287

    Article  PubMed  Google Scholar 

  9. Aarnio M, Mustonen H, Mecklin JP, Järvinen HJ (1998) Prognosis of colorectal cancer varies in different high-risk conditions. Ann Med 30(1):75–80

    Article  CAS  PubMed  Google Scholar 

  10. Lavery IC, Chiulli RA, Jagelman DG, Fazio VW, Weakley FL (1982) Survival with carcinoma arising in mucosal ulcerative colitis. Ann Surg 195(4):508–512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Gyde SN, Prior P, Thompson H, Waterhouse JA, Allan RN (1984) Survival of patients with colorectal cancer complicating ulcerative colitis. Gut 25(3):228–231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Watanabe T, Konishi T, Kishimoto J, Kotake K, Muto T, Sugihara K (2011) Ulcerative colitis-associated colorectal cancer shows a poorer survival than sporadic colorectal cancer: a nationwide Japanese study. Inflamm Bowel Dis 17(3):802–808

    Article  PubMed  Google Scholar 

  13. Delaunoit T, Limburg PJ, Goldberg RM, Lymp JF, Loftus EV (2006) Colorectal cancer prognosis among patients with inflammatory bowel disease. Clin Gastroenterol Hepatol 4(3):335–342

    Article  PubMed  Google Scholar 

  14. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, Moher D, Becker BJ, Sipe TA, Thacker SB, Meta-analysis of Observational Studies in Epidemiology (MOOSE) group (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. JAMA 283(15):2008–2012

    Article  CAS  PubMed  Google Scholar 

  15. DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7(3):177–188

    Article  CAS  PubMed  Google Scholar 

  16. Clancy C, Burke JP, Barry M, Kalady MF, Calvin Coffey J (2014) A meta-analysis to determine the effect of primary tumor resection for stage IV colorectal cancer with unresectable metastases on patient survival. Ann Surg Oncol 21(12):3900–3908

    Article  PubMed  Google Scholar 

  17. Lau J, Ioannidis JP, Schmid CH (1997) Quantitative synthesis in systematic reviews. Ann Intern Med 127(9):820–826

    Article  CAS  PubMed  Google Scholar 

  18. Clancy C, Burke JP, Coffey JC (2013) KRAS mutation does not predict the efficacy of neo-adjuvant chemoradiotherapy in rectal cancer: a systematic review and meta-analysis. Surg Oncol 22(2):105–111

    Article  PubMed  Google Scholar 

  19. Ali RA, Dooley C, Comber H, Newell J, Egan LJ (2011) Clinical features, treatment, and survival of patients with colorectal cancer with or without inflammatory bowel disease. Clin Gastroenterol Hepatol 9(7):584–589 e1-2

    Article  PubMed  Google Scholar 

  20. Bansal P, Sonnenberg A (1996) Risk factors of colorectal cancer in inflammatory bowel disease. Am J Gastroenterol 91(1):44–48

    CAS  PubMed  Google Scholar 

  21. Gearhart SL, Nathan H, Pawlik TM, Wick E, Efron J, Shore AD (2012) Outcomes from IBD-associated and non -IBD-associated colorectal cancer: a surveillance epidemiology and end results medicare study. Dis Colon rectum 55(3):270–277

  22. Greenstein AJ, Slater G, Heimann TM, Sachar DB, Aufses AH (1986) A comparison of multiple synchronous colorectal cancer in ulcerative colitis, familial polyposis coli, and de novo cancer. Ann Surg 203(2):123–128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Hamilton SR (1985) Colorectal carcinoma in patients with Crohn’s disease. Gastroenterology 89(2):398–407

    Article  CAS  PubMed  Google Scholar 

  24. Hughes RG, Hall TJ, Block GE, Levin B, Moossa AR (1978) The prognosis of carcinoma of the colon and rectum complicating ulcerative colitis. Surg Gynecol Obstet 146(1):46–48

    CAS  PubMed  Google Scholar 

  25. Hulten L, Kewenter J, Ahren C, Ojerskog B (1979) Clinical and morphological characteristics of colitis carcinoma and colorectal carcinoma in young people. Scand J Gastroenterol 14(6):673–678

    Article  CAS  PubMed  Google Scholar 

  26. Kiran RP, Khoury W, Church JM, Lavery IC, Fazio VW, Remzi FH (2010) Colorectal cancer complicating inflammatory bowel disease: similarities and differences between Crohn’s and ulcerative colitis based on three decades of experience. Ann Surg 252(2):330–335

    Article  PubMed  Google Scholar 

  27. Leowardi C, Schneider ML, Hinz U, Harnoss JM, Tarantino I, Lasitschka F, Ulrich A, Büchler MW, Kadmon M (2016) Prognosis of ulcerative colitis-associated colorectal carcinoma compared to sporadic colorectal carcinoma: a matched pair analysis. Ann Surg Oncol 23(3):870–876

    Article  PubMed  Google Scholar 

  28. Ohman U (1982) Colorectal carcinoma in patients with ulcerative colitis. Am J Surg 144(3):344–349

    Article  CAS  PubMed  Google Scholar 

  29. Ording AG, Horvath-Puho E, Erichsen R, Long MD, Baron JA, Lash TL, Sørensen HT (2013) Five-year mortality in colorectal cancer patients with ulcerative colitis or Crohn’s disease: a nationwide population-based cohort study. Inflamm Bowel Dis 19(4):800–805

    Article  PubMed  Google Scholar 

  30. Renz BW, Thasler WE, Preissler G, Heide T, Khalil PN, Mikhailov M, Jauch KW, Kreis ME, Rentsch M, Kleespies A (2013) Clinical outcome of IBD-associated versus sporadic colorectal cancer: a matched-pair analysis. J Gastrointest Surg 17(5):981–990

    Article  PubMed  Google Scholar 

  31. Ritchie JK, Hawley PR, Lennard-Jones JE (1981) Prognosis of carcinoma in ulcerative colitis. Gut 22(9):752–755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Shaukat A, Salfiti NI, Virnig DJ, Howard DH, Sitaraman SV, Liff JM, Lederle FA (2012) Is ulcerative colitis associated with survival among older persons with colorectal cancer in the US? A population-based case-control study. Dig Dis Sci 57(6):1647–1651

    Article  PubMed  Google Scholar 

  33. Shu X, Ji J, Sundquist J, Sundquist K, Hemminki K (2011) Survival in cancer patients hospitalized for inflammatory bowel disease in Sweden. Inflamm Bowel Dis 17(3):816–822

    Article  PubMed  Google Scholar 

  34. Gyde S, Prior P, Dew MJ, Saunders V, Waterhouse JA, Allan RN (1982) Mortality in ulcerative colitis. Gastroenterology 83(1 Pt 1):36–43

    CAS  PubMed  Google Scholar 

  35. Risques RA, Lai LA, Himmetoglu C, Ebaee A, Li L, Feng Z, Bronner MP, Al-Lahham B, Kowdley KV, Lindor KD, Rabinovitch PS, Brentnall TA (2011) Ulcerative colitis-associated colorectal cancer arises in a field of short telomeres, senescence, and inflammation. Cancer Res 71(5):1669–1679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Leedham SJ, Graham TA, Oukrif D, McDonald SA, Rodriguez-Justo M, Harrison RF, Shepherd NA, Novelli MR, Jankowski JA, Wright NA (2009) Clonality, founder mutations, and field cancerization in human ulcerative colitis-associated neoplasia. Gastroenterology 136(2):542–550.e6

    Article  PubMed  Google Scholar 

  37. Ullman TA, Itzkowitz SH (2011) Intestinal inflammation and cancer. Gastroenterology 140(6):1807–1816

    Article  CAS  PubMed  Google Scholar 

  38. Bossard C, Denis MG, Bezieau S, Bach-Ngohou K, Bourreille A, Laboisse CL, Mosnier JF (2007) Involvement of the serrated neoplasia pathway in inflammatory bowel disease-related colorectal oncogenesis. Oncol Rep 18(5):1093–1097

    PubMed  Google Scholar 

  39. Burmer GC, Rabinovitch PS, Haggitt RC, Crispin DA, Brentnall TA, Kolli VR, Stevens AC, Rubin CE (1992) Neoplastic progression in ulcerative colitis: histology, DNA content, and loss of a p53 allele. Gastroenterology 103(5):1602–1610

    Article  CAS  PubMed  Google Scholar 

  40. Juni P, Altman DG, Egger M (2001) Systematic reviews in health care: assessing the quality of controlled clinical trials. BMJ 323(7303):42–46

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John P. Burke.

Ethics declarations

Disclaimer

No funding or financial assistance were received by the authors.

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Reynolds, I., O’Toole, A., Deasy, J. et al. A meta-analysis of the clinicopathological characteristics and survival outcomes of inflammatory bowel disease associated colorectal cancer. Int J Colorectal Dis 32, 443–451 (2017). https://doi.org/10.1007/s00384-017-2754-3

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00384-017-2754-3

Keywords

Navigation