Breast, cervical and colorectal cancer screening in adults with diabetes: a systematic review and meta-analysis
Individuals with diabetes are at increased risk of developing and dying from cancer. Evidence-based guidelines recommend universal screening for breast, cervical and colorectal cancer; however, evidence on the uptake of these tests in individuals with diabetes is mixed. We conducted a meta-analysis to quantify the association between diabetes and participation in breast, cervical and colorectal cancer screening.
MEDLINE, EMBASE and CINAHL were searched systematically for publications between 1 January 1997 and 18 July 2018. The search was supplemented by handsearching of reference lists of the included studies and known literature reviews. Abstracts and full texts were assessed in duplicate according to the following eligibility criteria: study conducted in the general population; diabetes included as a predictor vs a comparison group without diabetes; and breast (mammography), cervical (Papanicolaou smear) or colorectal (faecal and endoscopic tests) cancer screening uptake included as an outcome. Random-effects meta-analyses were performed using the most-adjusted estimates for each cancer site.
Thirty-seven studies (25 cross-sectional, 12 cohorts) were included, with 27 studies on breast, 19 on cervical and 18 on colorectal cancer screening. Having diabetes was associated with significantly lower likelihood of breast (adjusted OR 0.83 [95% CI 0.77, 0.90]) and cervical (OR 0.76 [95% CI 0.71, 0.81]) cancer screening, relative to not having diabetes. Colorectal cancer screening was comparable across groups with and without diabetes (OR 0.95 [95% CI 0.86, 1.06]); however, women with diabetes were less likely to receive a colorectal cancer screening test than women without diabetes (OR 0.86 [95% CI 0.77, 0.97]).
Our findings suggest that women with diabetes have suboptimal breast, cervical and colorectal cancer screening rates, compared with women without diabetes, although the absolute differences might be modest. Given the increased risk of cancer in this population, higher quality prospective evidence is necessary to evaluate the contribution of diabetes to cancer screening disparities in relation to other patient-, provider- and system-level factors.
PROSPERO registration ID CRD42017073107.
KeywordsBreast cancer Cancer screening Cervical cancer Colorectal cancer Diabetes management Diabetes mellitus Healthcare barriers Healthcare disparities Meta-analysis Systematic review
Faecal immunochemical test
Faecal occult blood test
Randomised controlled trial
We would like to thank V. Lui (Gerstein Science Information Centre, University of Toronto) for her guidance in the design of the electronic database search strategy. DB is supported by the Enid Walker Award in Women’s Health Research from Women’s College Hospital. LL is supported by the Diabetes Investigator Award from Diabetes Canada.
DB, IL and LL conceived and designed the study. WW provided methodological and statistical advice. IL and LL provided clinical guidance in interpreting the results. DB, WW and IL assessed citations for eligibility and risk of bias. DB was involved in data abstraction, synthesis and drafting of the first version of the manuscript. All authors contributed critically to subsequent revisions and approved the final manuscript. All authors had full access to the data in the study and take responsibility for the integrity of the data and accuracy of the data analysis. The corresponding author attests that all listed authors meet authorship criteria and that no others meeting the criteria have been omitted.
This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors.
Duality of interest
The authors declare that there is no duality of interest associated with this manuscript.
- 10.Worndl E, Fung K, Fischer HD, Austin PC, Krzyzanowska MK, Lipscombe LL (2018) Preventable diabetic complications after a cancer diagnosis in patients with diabetes: a population-based cohort study. JNCI Cancer Spectr 2(1) pky008. Available from: https://academic.oup.com/jncics/article/doi/10.1093/jncics/pky008/4995319, accessed 14 Nov 2018
- 11.van de Poll-Franse LV, Houterman S, Janssen-Heijnen MLG, Dercksen MW, Coebergh JWW, Haak HR (2007) Less aggressive treatment and worse overall survival in cancer patients with diabetes: a large population based analysis. Int J Cancer 120(9):1986–1992. https://doi.org/10.1002/ijc.22532 CrossRefPubMedGoogle Scholar
- 13.Clark AM, Raine K, Raphael D (2004) The American Cancer Society, American Diabetes Association, and American Heart Association joint statement on preventing cancer, cardiovascular disease, and diabetes: where are the social determinants? Diabetes Care 27(12):3024–3024. https://doi.org/10.2337/diacare.27.12.3024 CrossRefPubMedGoogle Scholar
- 15.World Cancer Research Fund/American Institute for Cancer Research (2007) Food, nutrition, physical activity, and the prevention of cancer: a global perspective. AICR, Washington DCGoogle Scholar
- 19.Schienkiewitz A, Schulze MB, Hoffmann K, Kroke A, Boeing H Body mass index history and risk of type 2 diabetes: results from the European Prospective Investigation into Cancer and Nutrition (EPIC)-Potsdam study. Am J Clin Nutr 84(2):427–433. https://doi.org/10.1093/ajcn/84.2.427 CrossRefGoogle Scholar
- 23.Johnson JA, Carstensen B, Witte D et al (2012) on behalf of the Diabetes and Cancer Research Consortium. Diabetes and cancer (1): evaluating the temporal relationship between type 2 diabetes and cancer incidence. Diabetologia 55(6):1607–1618. https://doi.org/10.1007/s00125-012-2525-1 CrossRefGoogle Scholar
- 24.Gøtzsche PC, Jørgensen KJ (2013) Screening for breast cancer with mammography. Cochrane Database Syst Rev. Available from http://doi.wiley.com/10.1002/14651858.CD001877.pub5, accessed 14 November 2018
- 25.Peirson L, Fitzpatrick-Lewis D, Ciliska D, Warren R (2013) Screening for cervical cancer: a systematic review and meta-analysis. Syst Rev. 2:35. Available from: http://systematicreviewsjournal.biomedcentral.com/articles/10.1186/2046-4053-2-35, accessed 14 November 2018
- 31.Moyer VA (2012) Screening for cervical cancer: U.S. preventive services task force recommendation statement. Ann Intern Med 156(12):880. https://doi.org/10.7326/0003-4819-156-12-201206190-00424 CrossRefPubMedGoogle Scholar
- 32.Saslow D, Solomon D, Lawson HW et al (2012) American Cancer Society, American Society for Colposcopy and Cervical Pathology, and American Society for Clinical Pathology screening guidelines for the prevention and early detection of cervical cancer. Am J Clin Pathol 137(4):516–542. https://doi.org/10.1309/AJCPTGD94EVRSJCG CrossRefPubMedGoogle Scholar
- 34.Bénard F, Barkun AN, Martel M, von Renteln D (2018) Systematic review of colorectal cancer screening guidelines for average-risk adults: summarizing the current global recommendations. World J Gastroenterol 24(1):124–138. https://doi.org/10.3748/wjg.v24.i1.124 CrossRefPubMedPubMedCentralGoogle Scholar
- 35.World Health Organization (2005) Cervix cancer screening. Available from: http://www.myilibrary.com?id=73529, accessed 14 November 2018
- 46.O’Connor AM, Perrault DJ (1995) Importance of physician’s role highlighted in survey of women’s breast screening practices. Can J Public Health Rev Can Santé Publique 86(1):42–45Google Scholar
- 50.Stroup DF (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. JAMA 283(15):2008. https://doi.org/10.1001/jama.283.15.2008
- 57.Higgins JPT, Green S (eds) (2011) Cochrane handbook for systematic reviews of interventions. Version 5.1.0 [updated March 2011]. The Cochrane Collaboration; 2011. Available from: http://handbook.Cochrane.org, accessed 25 February 2019
- 58.Wells GA, Shea B, O’Connell D, et al. (2019) The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Available from http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp, accessed 25 February 2019
- 60.Herzog R, Álvarez-Pasquin MJ, Díaz C, Del Barrio JL, Estrada JM, Gil Á (2013) Are healthcare workers’ intentions to vaccinate related to their knowledge, beliefs and attitudes? A systematic review. Available from http://bmcpublichealth.biomedcentral.com/articles/10.1186/1471-2458-13-154, accessed 26 February 2019
- 62.Barros AJ, Hirakata VN (2003) Alternatives for logistic regression in cross-sectional studies: an empirical comparison of models that directly estimate the prevalence ratio. Available from http://bmcmedresmethodol.biomedcentral.com/articles/10.1186/1471-2288-3-21, accessed 26 February 2019
- 65.Jensen LF, Pedersen AF, Andersen B, Vestergaard M, Vedsted P (2015) Non-participation in breast cancer screening for women with chronic diseases and multimorbidity: a population-based cohort study. Available from: http://www.biomedcentral.com/1471-2407/15/798, accessed 14 November 2018
- 72.Blustein J, Weiss LJ (1998) The use of mammography by women aged 75 and older: factors related to health, functioning, and age. J Am Geriatr Soc 46(8):941–996. https://doi.org/10.1111/j.1532-5415.1998.tb02746.x CrossRefPubMedGoogle Scholar
- 76.Banks E, Beral V, Cameron R, et al. (2002) Comparison of various characteristics of women who do and do not attend for breast cancer screening. Available from http://breast-cancer-research.biomedcentral.com/articles/10.1186/bcr418, accessed 14 November 2018
- 83.Porter NR, Eberth JM, Samson ME, Garcia-Dominic O, Lengerich EJ, Schootman M (2012) Diabetes status and being up-to-date on colorectal cancer screening. Behavioral Risk Factor Surveillance System. 2016. Available from http://www.cdc.gov/pcd/issues/2016/15_0391.htm, accessed 14 November 2018
- 87.Chuck KW, Hwang M, Choi KS, Suh M, Jun JK, Park B (2017) Cancer screening rate in people with diabetes in the Korean population: results from the Korea National Health and Nutrition Examination Survey 2007-2009. Epidemiol Health 39:e2017036. https://doi.org/10.4178/epih.e2017036 CrossRefPubMedPubMedCentralGoogle Scholar
- 88.Constantinou P, Dray-Spira R, Menvielle G (2016) Cervical and breast cancer screening participation for women with chronic conditions in France: results from a national health survey. Available from http://bmccancer.biomedcentral.com/articles/10.1186/s12885-016-2295-0, accessed 14 November 2018
- 89.Coughlin SS, Uhler RJ, Hall HI, Briss PA (2004) Nonadherence to breast and cervical cancer screening: what are the linkages to chronic disease risk? Prev Chronic Dis 1(1):1–15Google Scholar
- 93.Martinez-Huedo MA, Lopez de Andres A, Hernandez-Barrera V, Carrasco-Garrido P, Martinez Hernandez D, Jiménez-Garcia R (2012) Adherence to breast and cervical cancer screening in Spanish women with diabetes: associated factors and trend between 2006 and 2010. Diabetes Metab 38(2):142–148. https://doi.org/10.1016/j.diabet.2011.09.007 CrossRefPubMedGoogle Scholar
- 127.Coronado GD, Petrik AF, Vollmer WM et al (2018) Effectiveness of a mailed colorectal cancer screening outreach program in community health clinics: the STOP CRC cluster randomized clinical trial. JAMA Intern Med 178(9):1174. https://doi.org/10.1001/jamainternmed.2018.3629 CrossRefPubMedPubMedCentralGoogle Scholar
- 128.Verdoodt F, Jentschke M, Hillemanns P, Racey CS, Snijders PJF, Arbyn M (2015) Reaching women who do not participate in the regular cervical cancer screening programme by offering self-sampling kits: a systematic review and meta-analysis of randomised trials. Eur J Cancer 51(16):2375–2385. https://doi.org/10.1016/j.ejca.2015.07.006 CrossRefPubMedGoogle Scholar
- 129.Dijkstra MG, van Zummeren M, Rozendaal L et al (2016) Safety of extending screening intervals beyond five years in cervical screening programmes with testing for high risk human papillomavirus: 14 year follow-up of population based randomised cohort in the Netherlands. BMJ 355:i4924Google Scholar
- 135.Horný M, Glover W, Gupte G, Saraswat A, Vimalananda V, Rosenzweig J (2017) Patient navigation to improve diabetes outpatient care at a safety-net hospital: a retrospective cohort study. Available from: https://bmchealthservres.biomedcentral.com/articles/10.1186/s12913-017-2700-7, accessed 14 November 2018