Cited by 1,105Pancreatic and Hepatic Oncology ResearchMetabolism, Diabetes, and CancerCancer Risks and Factors

Type-II diabetes and pancreatic cancer: a meta-analysis of 36 studies

Open access
Huxley, R, Ansary-Moghaddam, A, Berrington de González, A, Barzi, F, Woodward, M·2005·British Journal of Cancer

Abstract

Pancreatic cancer is the eighth major form of cancer-related death worldwide, causing 227 000 deaths annually. Type-II diabetes is widely considered to be associated with pancreatic cancer, but whether this represents a causal or consequential association is unclear. We conducted a meta-analysis to examine this association. A computer-based literature search from 1966 to 2005 yielded 17 case-control and 19 cohort or nested case-control studies with information on 9220 individuals with pancreatic cancer. The age and sex-adjusted odds ratio (OR) for pancreatic cancer associated with type-II diabetes was obtained from each study. The combined summary odds ratio was 1.82 (95% confidence interval (95% CI) 1.66-1.89), with evidence of heterogeneity across the studies (P=0.002 for case-control and P=0.05 for cohort studies) that was explained, in part, by higher risks being reported by smaller studies and studies that reported before 2000. Individuals in whom diabetes had only recently been diagnosed (< 4 years) had a 50% greater risk of the malignancy compared with individuals who had diabetes for > or =5 years (OR 2.1 vs 1.5; P=0.005). These results support a modest causal association between type-II diabetes and pancreatic cancer.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/sj.bjc.6602619

Cites

4 of 4 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • More than 50% of PDAC is accompanied by diabetes at the time of diagnosis.

    “and more than 50% of PDAC is accompanied by diabetes at the time of diagnosis.212”

    From Artificial Intelligence and Early Detection of Pancreatic Cancer: 2020 Summative Review (2021) · cites this paper as [212]

    The paper’s introductory passage says type-II diabetes frequently occurs with pancreatic cancer, and the Discussion describes diabetes diagnosed shortly before the malignancy. Neither passage gives the proportion of pancreatic cancer patients with diabetes at diagnosis, so the claim that it exceeds 50% is unsupported. The paper’s 50% figures concern relative risk, not prevalence. (LLM, conf=0.82)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 55

  1. Adami H-O, McLaughlin J, Ekbom A (1994) Cancer risk in patients with diabetes mellitus. Cancer Causes Control 2: 307–314 1932543
  2. Anderson KE, Johnson TW, Lazovich D, Folsom AR (2002) Association between nonsteroidal anti-inflammatory drug use and the incidence of pancreatic cancer. J Nat Cancer Inst 94: 1168–1171 12165642
  3. Baghurst PA, McMichael AJ, Slavotinek AH, Baghurst KI, Boyle P, Walker AM (1991) A case–control study of diet and cancer of the pancreas. Am J Epidemiol 134: 167–179 1862800
  4. Balkau B, Barrett-Connor E, Eschwege E, Richard J-L, Claude J-R, Ducimetiere P (1993) Diabetes and pancreatic cancer. Diab Metab 19: 458–462 8056126
  5. Batty GD, Shipley MJ, Marmot M, Smith GD (2004) Diabetes status and post-load plasma glucose concentration in relation to site-specific cancer mortality: findings from the original Whitehall study. Cancer Causes Control 15: 873–881 15577289
  6. Berrington de Gonzalez A, Sweetland S, Spencer E (2003) A meta-analysis of obesity and the risk of pancreatic cancer. Br J Cancer 89: 519–523 12888824 PMC2394383
  7. Bonelli L, Aste H, Bovo P, Cavallini G, Felder M, Gusmaroli R, Morandini E, Ravelli P, Briglia R, Lombardo L, De Micheli A, Pugliese V (2003) Exocrine pancreatic cancer, cigarette smoking, and diabetes mellitus: a case–control study in northern Italy. Pancreas 27: 143–149 12883263
  8. Bueno de Mesquita HB, Maisonneuve P, Moerman CJ, Walker AM (1992) Aspects of medical history and exocrine carcinoma of the pancreas: a population-based case–control study in the Netherlands. Int J Cancer 52: 17–23 1500222
  9. Calle EE, Murphy TK, Rodriguez C, Thun MJ, Heath WC (1998) Diabetes mellitus and pancreatic cancer mortality in a prospective cohort of US adults. Canc Causes Contr 9: 403–410 9794172
  10. Chow WH, Gridley G, Nyren O, Linet MS, Ekbom A, Fraumeni Jr JF, Adami HO (1995) Risk of pancreatic cancer following diabetes mellitus: a nationwide cohort study in Sweden. J Nat Canc Inst 87: 930–931 7666483
  11. Coughlin SS, Calle EE, Patel AV, Thun MJ (2000) Predictors of pancreatic cancer mortality among a large cohort of United States adults. Cancer Causes Control 11: 915–923 11142526
  12. Coughlin SS, Calle EE, Teras LR, Petrelli J, Thun MJ (2004) Diabetes mellitus as a predictor of cancer mortality in a large cohort of US adults. Am J Epidemiol 159: 1160–1167 15191933
  13. Cull CA, Neil HA, Holman RR (2004) Changing aspirin use in patients with Type 2 diabetes in the UKPDS. Diab Med 21: 1368–1371 15569143
  14. Cuzick J, Babiker AG (1989) Pancreatic cancer, alcohol, diabetes mellitus and gall-bladder disease. Int J Cancer 43: 415–421 2925272
  15. Davey Smith G, Bracha Y, Svendsen KH, Neaton JD, Haffner SM, Kuller LH (2005) Multiple Risk Factor Intervention Trial Research Group. Incidence of type 2 diabetes in the randomized multiple risk factor intervention trial. Ann Intern Med 142: 313–322 15738450
  16. Davey Smith G, Egger M, Shipley MJ, Marmot MG (1992) Post-challenge glucose concentration, impaired glucose tolerance, diabetes and cancer mortality in men. Am J Epidemiol 136: 1110–1114 1462971
  17. Doll R, Peto R (1976) Mortality in relation to smoking: 20 years observation on male British doctors. Br Med J 2: 1525–1536 1009386 PMC1690096
  18. Ekoe JM, Ghadirian P, Simard A, Baillargeon J, Perret C (1992) Diabete sucre et cancer du pancreas: une etude cas-temoins dans le grand Montreal, Quebec, Canada. Rev Epidemiol Sante Publ 40: 447–453 1287744
  19. Everhart J, Wright D (1995) Diabetes mellitus as a risk factor for pancreatic cancer: a meta-analysis. JAMA 273: 1605–1609 7745774
  20. Farrow DC, Davis S (1990) Risk of pancreatic cancer in relation to medical history and the use of tobacco, alcohol and coffee. Int J Cancer 45: 816–820 2335385
  21. Friedman GD, Van Den Eeden SK (1993) Risk factors for pancreatic cancer: an exploratory study. Int J Epidemiol 22: 30–37 8449644
  22. Frye JN, Inder WJ, Dobbs BR, Frizelle FA (2000) Pancreatic cancer and diabetes: is there a relationship? A case-controlled study. Aust NZ J Surg 70: 722–724 11021485
  23. Gapstur SM, Gann PH, Lowe W, Liu K, Colangelo L, Dyer A (2000) Abnormal glucose metabolism and pancreatic cancer mortality. JAMA 283: 2552–2558 10815119
  24. Gold EB, Gordis L, Diener MD (1985) Diet and other risk factors for cancer of the pancreas. Cancer 55: 460–467 3965101
  25. Gullo L, Pezzilli R, Morselli-Labate AM, for the Italian Pancreatic Cancer Study Group (1994) Diabetes and the risk of pancreatic cancer. N Engl J Med 331: 81–84 8208269
  26. Hiatt RA, Klatsky AL, Armstrong MA (1988) Pancreatic cancer, blood glucose and beverage consumption. Int J Cancer 41: 794–797 3372055
  27. Inoue M, Tajima K, Takezaki T, Hamajima N, Hirose K, Ito H, Tominaga S (2003) Epidemiology of pancreatic cancer in Japan: a nested case–control study from the Hospital-based Epidemiologic Research Program at Aichi Cancer Center (HERPACC). Inter J Epidemiol 32: 257–262 12714546
  28. Jain M, Howe GR, St Loluis P, Miller AB (1991) Coffee and alcohol as determinants of risk of pancreas cancer: a case–control study from Toronto. Int J Cancer 47: 384–389 1993545
  29. Jee SH, Ohrr H, Sull JW, Yun JE, Ji M, Samet JM (2005) Fasting serum glucose level and cancer risk in Korean men and women. JAMA 293: 194–202 15644546
  30. Kalapothaki V, Tzonou A, Hsieh C-C, Toupadaki N, Karakatsani A, Trichopoulos D (1993) Tobacco, ethanol, coffee, pancreatitis, diabetes mellitus, and cholelithiasis as risk factors for pancreatic carcinoma. Cancer Causes Control 4: 375–382 8347787
  31. Kessler II (1970) Cancer mortality among diabetics. J Nat Cancer Inst 44: 673–686 11515436
  32. La Vecchia C, Negri E, D'Avanzo B, Ferraroni M, Gramenzi A, Savoldelli R, Boyle P, Franceschi S (1990) Medical history, diet and pancreatic cancer. Oncology 47: 463–466 2243664
  33. La Vecchia C, Negri E, Franceschi S, D'Auanzo B, Boyle P (1994) A case–control study of diabetes mellitus and cancer risk. Br J Cancer 70: 950–953 7947103 PMC2033532
  34. Lee CT, Chang FY, Lee SD (1996) Risk factors for pancreatic cancer in orientals. J Gastroenterol Hepatol 11: 491–495 8743923
  35. Lin RS, Kessler II (1981) A multifactorial model for pancreatic cancer in man: epidemiologic evidence. JAMA 245: 147–152 7452829
  36. Lin Y, Tamakoshi A, Kawamura T, Inaba Y, Kikuchi S, Motohashi Y, Kurosawa M, Ohno Y (2002) Risk of pancreatic cancer in relation to alcohol drinking, coffee consumption and medical history: findings from the Japan collaborative cohort study for evaluation of cancer risk. Inter J Cancer 99: 742–746 12115510
  37. Lund Nilsen TI, Johnsen R, Vatten LJ (2000) Socio-economic and lifestyle factors associated with the risk of prostate cancer. Br J Cancer 82: 1358–1363 10755415 PMC2374496
  38. Martinenghi S, Dell'Antonio G, Secchi A, Di Carlo V, Pozza G (1997) Cancer arising after pancreas and/or kidney transplantation in a series of 99 diabetic patients. Diabetes Care 20: 272–275 9051370
  39. Mihara T, Oohashi H, Hirata Y (1986) Mortality of Japanese diabetics in a seven-year follow-up study. Diabetes Res Clin Pract 2: 139–144 3743361
  40. Mills PK, Beeson WL, Abbey DE, Fraser GE, Phillips RL (1988) Dietary habits and past medical history as related to fatal pancreas cancer risk among Adventists. Cancer 61: 2578–2585 3365678
  41. Norell S, Ahlbom A, Erwald R (1986) Diabetes, gall stone disease, and pancreatic cancer. Br J Cancer 54: 377–378 3741772 PMC2001526
  42. O'Mara BA, Byers T, Schoenfeld E (1985) Diabetes mellitus and cancer risk: a multisite case–control study. J Chron Dis 38: 435–441 3998058
  43. Parkin DM, Bray F, Ferlay J, Pisani P (2002) Global cancer statistics, 2002. CA Cancer J Clin 55: 74–108 15761078
  44. Permert J, Adrain TE, Jacobssen P, Jorfelt L, Fruin AB, Larsson J (1993) Is profound peripheral insulin resistance in patients with pancreatic cancer caused by a tumor-associated factor? Am J Surg 165: 61–67 8380314
  45. Ragozzino M, Melton LJ, Chu C-P, Palumbo PJ (1982) Subsequent cancer risk in the incidence cohort of Rochester, Minnesota, residents with diabetes mellitus. J Chron Dis 35: 13–19 7068798
  46. Rulyak SJ, Lowenfels AB, Maisonneuve P, Brentnall TA (2003) Risk factors for the development of pancreatic cancer in familial pancreatic cancer kindreds. Gastroenterology 124: 1292–1299 12730869
  47. Shibata A, Mack TM, Paganini-Hill A, Ross RK, Henderson BE (1994) A prospective study of pancreatic cancer in the elderly. Int J Cancer 58: 46–49 8014014
  48. Silverman DT (2001) Risk factors for pancreatic cancer: a case–control study based on direct interviews. Teratogen Carcinogen Mutagen 21: 7–25 11135318
  49. Silverman DT, Schiffman M, Everhart J, Goldstein A, Lillemoe KD, Swanson GM, Schwartz AG, Brown LM, Greenberg RS, Schoenberg JB, Pottern LM, Hoover RN, Fraumeni Jr JF (1999) Diabetes mellitus, other medical conditions and familial history of cancer as risk factors for pancreatic cancer. Br J Cancer 80: 1830–1837 10468306 PMC2363127
  50. Stolzenberg-Solomon RZ, Pietinen P, Taylor PR, Virtamo J, Albanes D (2002) Prospective study of diet and pancreatic cancer in male smokers. Am J Epidemiol 155: 783–792 11978580
  51. Thun MJ, Namboodiri MM, Calle EE (1993) Aspirin use and risk of fatal cancer. Cancer Res 53: 1322–1327 8443812
  52. Wang F, Herrington M, Larsson J, Permert J (2003) The relationship between diabetes and pancreatic cancer. Mol Cancer 2: 4–8 12556242 PMC149418
  53. Whittemore AS, Paffenbarger RS, Anderson K, Halpern J (1983) Early precursors of pancreatic cancer in college men. J Chron Dis 36: 251–256 6826689
  54. Wynder EL, Mabuchi K, Maruchi N, Fortner JG (1973) Epidemiology of cancer of the pancreas. J Natl Cancer Inst 50: 645–667 4350660
  55. Zendehdel K, Nyren O, Ostenson C-G, Adami H-O, Ekbom A, Ye W (2003) Cancer incidence in patients with type 1 diabetes mellitus: a population-based cohort study in Sweden. J Nat Canc Inst 95: 1797–1800 14652242

Cited by

Sorted by citations

Authors
Huxley, R., Ansary-Moghaddam, A., Berrington de González, A., Barzi, F., & Woodward, M.
Affiliations
The University of Sydney (AU)
Corresponding author
Huxley, R
Venue
British Journal of Cancer
Published
2005-05-10
Volume
92
Issue
11
Pages
2076-2083
ISSN
  • 0007-0920 (ISSN-L)
  • 1532-1827
OpenAlex
W2066809635
Cited by
1,105
References
4
Citations by year
2026: 23 · 2025: 33 · 2024: 22 · 2023: 41 · 2022: 45 · 2021: 47 · 2020: 50 · 2019: 54 · 2018: 53 · 2017: 59 · 2016: 61 · 2015: 69 · 2014: 70 · 2013: 85 · 2012: 82
FWCI
3.49
Type
journal article
Language
en
Open access
Locations
  • British Journal of Cancer (publishedVersion, cc-by-nc-sa)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Topics
  • Health Sciences › Medicine › Oncology › Pancreatic and Hepatic Oncology Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
  • Health Sciences › Medicine › Oncology › Cancer Risks and Factors
Keywords
type 2 diabetes, pancreatic cancer, diabetes and cancer risk, causal relationship, diabetes duration, pancreatic cancer risk factors
MeSH terms
Diabetes Mellitus, Type 2, Humans, Pancreatic Neoplasms, Risk Factors, Time Factors, Cohort Studies, Odds Ratio, Case-Control Studies

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review