The DOI matches its Crossref record; 19 of the 20 references it cites were found in a registry or an index.
Metformin Associated With Lower Cancer Mortality in Type 2 Diabetes
Open accessAbstract
OBJECTIVE: Several studies have suggested an association between specific diabetes treatment and cancer mortality. We studied the association between metformin use and cancer mortality in a prospectively followed cohort. RESEARCH DESIGN AND METHODS: In 1998 and 1999, 1,353 patients with type 2 diabetes were enrolled in the Zwolle Outpatient Diabetes project Integrating Available Care (ZODIAC) study in the Netherlands. Vital status was assessed in January 2009. Cancer mortality rate was evaluated using standardized mortality ratios (SMRs), and the association between metformin use and cancer mortality was evaluated with a Cox proportional hazards model, taking possible confounders into account. RESULTS: Median follow-up time was 9.6 years, average age at baseline was 68 years, and average A1C was 7.5%. Of the patients, 570 died, of which 122 died of malignancies. The SMR for cancer mortality was 1.47 (95% CI 1.22–1.76). In patients taking metformin compared with patients not taking metformin at baseline, the adjusted hazard ratio (HR) for cancer mortality was 0.43 (95% CI 0.23–0.80), and the HR with every increase of 1 g of metformin was 0.58 (95% CI 0.36–0.93). CONCLUSIONS: In general, patients with type 2 diabetes are at increased risk for cancer mortality. In our group, metformin use was associated with lower cancer mortality compared with nonuse of metformin. Although the design cannot provide a conclusion about causality, our results suggest a protective effect of metformin on cancer mortality.
Overview
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.
Integrity signals
Registry
Cites
Statistics
Verification
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.
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?
The cited source says what the claim attributes to it.
In the citing paper
“Several epidemiologic studies have shown that metformin use is associated with reduced cancer incidence and mortality (Landman et al., 2010; Lee et al., 2011; Libby et al., 2009; Monami et al., 2011; Tseng, 2012).”
From Metformin as a tool to target aging (2016) · cites this paper as Landman et al., 2010
In the citing paper
“The reduced risk of cancer and cancer mortality observed in these studies has been consistently in the range of 25% to 30% [135-139,145-147].”
From Metformin: An Old But Still the Best Treatment for Type 2 Diabetes (2013) · cites this paper as [138]
In the citing paper
“A prospective study (median follow-up time of 9.6 years) found that metformin use at baseline was associated with lower cancer-related mortality and that this association appeared to be dose dependent [138].”
From Metformin: An Old But Still the Best Treatment for Type 2 Diabetes (2013) · cites this paper as [138]
In the citing paper
“Metformin use is associated with lower cancer-related mortality.”
From Metformin: An Old But Still the Best Treatment for Type 2 Diabetes (2013) · cites this paper as [138]
In the citing paper
“Patients with type 2 diabetes who are prescribed metformin had a lower risk of cancer compared to patients who did not take it.”
From Metformin: An Old But Still the Best Treatment for Type 2 Diabetes (2013) · cites this paper as [138]
In the citing paper
“When compared to those on other treatments, metformin users had a lower risk of cancer. A dose-relationship has been reported [138,144,145].”
From Metformin: An Old But Still the Best Treatment for Type 2 Diabetes (2013) · cites this paper as [138]
In the citing paper
“Results of a growing number of observational human studies suggest that treatment with metformin (relative to other glucose-lowering therapies) is associated with reduced risk of cancer (89–93) or cancer mortality (94).”
From Diabetes and Cancer (2010) · cites this paper as [94]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Metformin and reduced risk of cancer in diabetic patients
Evans, J. M. M., Donnelly, L. A., Emslie-Smith, A. M., Alessi, D. R., & Morris, A. D. (2005) · BMJ · doi:10.1136/bmj.38415.708634.f7 · Cited by 2,388
The influence of glucose-lowering therapies on cancer risk in type 2 diabetes
Currie, C. J., Poole, C. D., & Gale, E. A. M. (2009) · Diabetologia · doi:10.1007/s00125-009-1440-6 · Cited by 1,124
New Users of Metformin Are at Low Risk of Incident Cancer
Libby, G., Donnelly, L. A., Donnan, P. T., Alessi, D. R., Morris, A. D., & Evans, J. M. M. (2009) · Diabetes Care · doi:10.2337/dc08-2175 · Cited by 996
Bowker, S. L., Majumdar, S. R., Veugelers, P., & Johnson, J. A. (2006) · Diabetes Care · doi:10.2337/diacare.29.02.06.dc05-1558 · Cited by 933
Jiralerspong, S., Palla, S. L., Giordano, S. H., Meric-Bernstam, F., Liedtke, C., Barnett, C. M., Hsu, L., Hung, M.-C., Hortobagyi, G. N., & Gonzalez-Angulo, A. M. (2009) · Journal of Clinical Oncology · doi:10.1200/jco.2009.19.6410 · Cited by 880 · cited 1×
“For example, type 2 diabetic patients receiving neoadjuvant chemotherapy for breast cancer as well as metformin were more likely to have a complete remission than patients not receiving metformin (14).”
Sahra, I. B., Laurent, K., Loubat, A., Giorgetti-Peraldi, S., Colosetti, P., Auberger, P., Tanti, J. F., Le Marchand-Brustel, Y., & Bost, F. (2008) · Oncogene · doi:10.1038/sj.onc.1211024 · Cited by 861
Diabetes Mellitus as a Predictor of Cancer Mortality in a Large Cohort of US Adults
Coughlin, S. S., Calle, E. E., Teras, L. R., Petrelli, J. M., & Thun, M. J. (2004) · American Journal of Epidemiology · doi:10.1093/aje/kwh161 · Cited by 795
Hemkens, L. G., Grouven, U., Bender, R., Günster, C., Gutschmidt, S., Selke, G. W., & Sawicki, P. T. (2009) · Diabetologia · doi:10.1007/s00125-009-1418-4 · Cited by 607
Antidiabetic Therapies Affect Risk of Pancreatic Cancer
Li, D., Yeung, S. J., Hassan, M. M., Konopleva, M., & Abbruzzese, J. L. (2009) · Gastroenterology · doi:10.1053/j.gastro.2009.04.013 · Cited by 584
Prospective Study of Adult Onset Diabetes Mellitus (Type 2) and Risk of Colorectal Cancer in Women
Hu, F. B., Manson, J. E., Liu, S., Hunter, D. J., Colditz, G. A., Michels, K. B., Speizer, F. E., & Giovannucci, E. L. (1999) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/91.6.542 · Cited by 420
Excess Risk of Primary Liver Cancer in Patients With Diabetes Mellitus
Adami, H., Chow, W.-H., Nyrén, O., Berne, C., Linet, M. S., Ekbom, A., Wolk, A., McLaughlin, J. K., & Fraumeni, J. F. (1996) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/88.20.1472 · Cited by 373
Insulin therapy and colorectal cancer risk among type 2 diabetes mellitus patients
Yang, Y., Hennessy, S., & Lewis, J. D. (2004) · Gastroenterology · doi:10.1053/j.gastro.2004.07.011 · Cited by 350
Wright, J. L., & Stanford, J. L. (2009) · Cancer Causes & Control · doi:10.1007/s10552-009-9407-y · Cited by 276
van der Burg, B., Rutteman, G. R., Blankenstein, M. A., de Laat, S. W., & van Zoelen, E. J. J. (1988) · Journal of Cellular Physiology · doi:10.1002/jcp.1041340112 · Cited by 247
Ventilation in Homes and Bronchial Obstruction in Young Children
Øie, L., Nafstad, P. H. J., Botten, G., Magnus, P. M., & Jaakkola, J. J. K. (1999) · Epidemiology · doi:10.1097/00001648-199905000-00018 · Cited by 186
Diabetes mellitus and pancreaticcancer mortality in a prospectivecohort of United States adults
Calle, E. E., Murphy, T. K., Rodriguez, C., Thun, M. J., & Heath, C. W. (1998) · Cancer Causes & Control · doi:10.1023/a:1008819701485 · Cited by 143
Risk of Pancreatic Cancer Following Diabetes Mellitus: a Nationwide Cohort Study in Sweden
Chow, W.-H., Gridley, G., Nyrén, O., Linet, M. S., Ekbom, A., Fraumeni, J. F., & Adami, H. (1995) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/87.12.930 · Cited by 127
Is Diabetes Mellitus Associated with Prostate Cancer Incidence and Survival?
Will, J. C., Vinicor, F., & Calle, E. E. (1999) · Epidemiology · doi:10.1097/00001648-199905000-00021 · Cited by 83
Shared care with task delegation to nurses for type 2 diabetes: prospective observational study.
Ubink-Veltmaat, L. J., Bilo, H. J. G., Groenier, K. H., Rischen, R., & Jong, B. M. (2005) · PubMed · Cited by 77
Self-citation
Flagged first, then by citations
1 of the 20 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Diabetes Mellitus, Fasting Glucose, and Risk of Cause-Specific Death
The Emerging Risk Factors Collaboration (2011) · New England Journal of Medicine · doi:10.1056/nejmoa1008862 · Cited by 2,726
Giovannucci, E., Harlan, D. M., Archer, M. C., Bergenstal, R. M., Gapstur, S. M., Habel, L. A., Pollak, M., Regensteiner, J. G., & Yee, D. (2010) · Diabetes Care · doi:10.2337/dc10-0666 · Cited by 2,366
Cellular and molecular mechanisms of metformin: an overview
Viollet, B., Guigas, B., Garcia, N. S., Leclerc, J., Foretz, M., & Andreelli, F. (2012) · Clinical Science · doi:10.1042/cs20110386 · Cited by 1,720
Metformin as a tool to target aging
Barzilai, N., Crandall, J. P., Kritchevsky, S. B., & Espeland, M. A. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2016.05.011 · Cited by 1,096
Diabetes and Cancer: A Consensus Report
Giovannucci, E. L., Harlan, D. M., Archer, M. C., Bergenstal, R. M., Gapstur, S. M., Habel, L. A., Pollak, M., Regensteiner, J. G., & Yee, D. (2010) · CA A Cancer Journal for Clinicians · doi:10.3322/caac.20078 · Cited by 1,082
Metadata
- Authors
- Landman, G. W. D., Kleefstra, N., van Hateren, K. J. J., Groenier, K. H., Gans, R. O. B., & Bilo, H. J. G.
- Affiliations
- Isala (NL)
- Diabetes Centre, Isala Clinics, Zwolle, the Netherlands;
- University Medical Center Groningen (NL)
- Corresponding author
- Landman, Gijs W.D.
- Venue
- Diabetes Care
- Publisher
- American Diabetes Association
- Published
- 2009-11-16
- Volume
- 33
- Issue
- 2
- Pages
- 322-326
- ISSN
- 0149-5992 (ISSN-L)
- 1935-5548
- PMC
- PMC2809274
- OpenAlex
- W2058725063
- Cited by
- 502
- References
- 20
- Citations by year
- 2026: 5 · 2025: 7 · 2024: 11 · 2023: 17 · 2022: 28 · 2021: 24 · 2020: 31 · 2019: 23 · 2018: 28 · 2017: 30 · 2016: 25 · 2015: 39 · 2014: 41 · 2013: 54 · 2012: 48
- FWCI
- 18.64
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc-nd
- Locations
- Diabetes Care (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (publishedVersion, other-oa)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, other-oa)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes Treatment and Management
- Health Sciences › Medicine › Oncology › Pancreatic and Hepatic Oncology Research
- Keywords
- metformin, cancer mortality, type 2 diabetes, diabetes drugs, cancer risk, standardized mortality ratio
- MeSH terms
- Aged, Blood Pressure, Diabetes Mellitus, Type 2, Diabetic Angiopathies, Female, Glycated Hemoglobin, Humans, Hypertension, Hypoglycemic Agents, Insulin, Male, Metformin, Middle Aged, Neoplasms, Netherlands, Prospective Studies, Risk Factors, Smoking, Cohort Studies, Body Mass Index
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
