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Diabetologia

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01-01-2020 | Breast Cancer

Breast, cervical and colorectal cancer screening in adults with diabetes: a systematic review and meta-analysis

Authors: Dominika Bhatia, Iliana C. Lega, Wei Wu, Lorraine L. Lipscombe

Published in: Diabetologia | Issue 1/2020

Abstract

Aims/hypothesis

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.

Methods

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.

Results

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]).

Conclusions/interpretation

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.

Registration

PROSPERO registration ID CRD42017073107.

Available only for authorised users

Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68(6):394–424. https://doi.org/10.3322/caac.21492 CrossRefPubMed

Tsilidis KK, Kasimis JC, Lopez DS, Ntzani EE, Ioannidis JPA (2015) Type 2 diabetes and cancer: umbrella review of meta-analyses of observational studies. BMJ 350:g7607. https://doi.org/10.1136/bmj.g7607 CrossRefPubMed

Larsson SC, Mantzoros CS, Wolk A (2007) Diabetes mellitus and risk of breast cancer: a meta-analysis. Int J Cancer 121(4):856–862. https://doi.org/10.1002/ijc.22717 CrossRefPubMed

Larsson SC, Orsini N, Wolk A (2005) Diabetes mellitus and risk of colorectal cancer: a meta-analysis. J Natl Cancer Inst 97(22):1679–1687. https://doi.org/10.1093/jnci/dji375 CrossRefPubMed

Barone BB, Yeh HC, Snyder CF et al (2008) Long-term all-cause mortality in cancer patients with preexisting diabetes mellitus: a systematic review and meta-analysis. JAMA 300(23):2754. https://doi.org/10.1001/jama.2008.824 CrossRefPubMedPubMedCentral

Lipscombe LL, Fischer HD, Austin PC et al (2015) The association between diabetes and breast cancer stage at diagnosis: a population-based study. Breast Cancer Res Treat 150(3):613–620. https://doi.org/10.1007/s10549-015-3323-5 CrossRefPubMed

Peairs KS, Barone BB, Snyder CF et al (2011) Diabetes mellitus and breast cancer outcomes: a systematic review and meta-analysis. J Clin Oncol 29(1):40–46. https://doi.org/10.1200/JCO.2009.27.3011 CrossRefPubMed

Fleming ST, Pursley HG, Newman B, Pavlov D, Chen K (2005) Comorbidity as a predictor of stage of illness for patients with breast cancer. Med Care 43(2):132–140. https://doi.org/10.1097/00005650-200502000-00006 CrossRefPubMed

Srokowski TP, Fang S, Hortobagyi GN, Giordano SH (2009) Impact of diabetes mellitus on complications and outcomes of adjuvant chemotherapy in older patients with breast cancer. J Clin Oncol 27(13):2170–2176. https://doi.org/10.1200/JCO.2008.17.5935 CrossRefPubMedPubMedCentral

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 CrossRefPubMed

12.

Gross CP, McAvay GJ, Guo Z, Tinetti ME (2007) The impact of chronic illnesses on the use and effectiveness of adjuvant chemotherapy for colon cancer. Cancer 109(12):2410–2419. https://doi.org/10.1002/cncr.22726 CrossRefPubMed

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 CrossRefPubMed

14.

Davidson LE, Hudson R, Kilpatrick K et al (2009) Effects of exercise modality on insulin resistance and functional limitation in older adults: a randomized controlled trial. JAMA Intern Med 169(2):122–131CrossRef

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 DC

16.

Barclay AW, Petocz P, McMillan-Price J et al (2008) Glycemic index, glycemic load, and chronic disease risk—a meta-analysis of observational studies. Am J Clin Nutr 87(3):627–637. https://doi.org/10.1093/ajcn/87.3.627 CrossRefPubMed

17.

Sasco AJ, Secretan MB, Straif K (2004) Tobacco smoking and cancer: a brief review of recent epidemiological evidence. Lung Cancer 45:S3–S9. https://doi.org/10.1016/j.lungcan.2004.07.998 CrossRefPubMed

18.

Renehan AG, Tyson M, Egger M, Heller RF, Zwahlen M (2008) Body-mass index and incidence of cancer: a systematic review and meta-analysis of prospective observational studies. Lancet 37(9612):569-578CrossRef

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 CrossRefPubMed

20.

Pischon T, Lahmann PH, Boeing H et al (2006) Body size and risk of colon and rectal cancer in the European prospective investigation into cancer and nutrition (EPIC). J Natl Cancer Inst 98(13):920–931. https://doi.org/10.1093/jnci/djj246 CrossRefPubMed

21.

Pisani P (2008) Hyper-insulinaemia and cancer, meta-analyses of epidemiological studies. Arch Physiol Biochem 114(1):63–70. https://doi.org/10.1080/13813450801954451 CrossRefPubMed

22.

Goodwin PJ (2008) Insulin in the adjuvant breast cancer setting: a novel therapeutic target for lifestyle and pharmacologic interventions? J Clin Oncol 26(6):833–834. https://doi.org/10.1200/JCO.2007.14.7132 CrossRefPubMed

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 CrossRefPubMed

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

26.

Lin JS, Piper MA, Perdue LA et al (2016) Screening for colorectal cancer: updated evidence report and systematic review for the US Preventive Services Task Force. JAMA 315(23):2576. https://doi.org/10.1001/jama.2016.3332 CrossRefPubMed

27.

Siu AL, on behalf of the U.S. Preventive Services Task Force (2016) Screening for breast cancer: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med 164(4):279–296CrossRefPubMed

28.

Oeffinger KC, Fontham ETH, Etzioni R et al (2015) Breast cancer screening for women at average risk: 2015 guideline update from the American Cancer Society. JAMA 314(15):1599–1614. https://doi.org/10.1001/jama.2015.12783 CrossRefPubMedPubMedCentral

29.

The Canadian Task Force on Preventive Health Care (2011) Recommendations on screening for breast cancer in average-risk women aged 40-74 years. Can Med Assoc J 183(17):1991–2001. https://doi.org/10.1503/cmaj.110334 CrossRef

30.

Lauby-Secretan B, Scoccianti C, Loomis D et al (2015) Breast-cancer screening: viewpoint of the IARC Working Group. N Engl J Med 372(24):2353–2358CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

33.

Canadian Task Force on Preventive Health Care (2013) Recommendations on screening for cervical cancer. Can Med Assoc J 185(1):35–45. https://doi.org/10.1503/cmaj.121505 CrossRef

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 CrossRefPubMedPubMedCentral

35.

World Health Organization (2005) Cervix cancer screening. Available from: http://www.myilibrary.com?id=73529, accessed 14 November 2018

36.

Dowling EC, Klabunde C, Patnick J, Ballard-Barbash R, for The International Cancer Screening Network (ICSN). Breast and cervical cancer screening programme implementation in 16 countries. J Med Screen 2010;17(3):139–146. https://doi.org/10.1258/jms.2010.010033 CrossRefPubMed

37.

Williams JH, Carter SM, Rychetnik L (2014) ‘Organised’ cervical screening 45 years on: how consistent are organised screening practices? Eur J Cancer 50(17):3029–3038. https://doi.org/10.1016/j.ejca.2014.09.005 CrossRefPubMed

38.

Benson VS, Patnick J, Davies AK, Nadel MR, Smith RA, Atkin WS (2008) Colorectal cancer screening: a comparison of 35 initiatives in 17 countries: worldwide colorectal Cancer screening. Int J Cancer 122(6):1357–1367. https://doi.org/10.1002/ijc.23273 CrossRefPubMed

39.

Schreuders EH, Ruco A, Rabeneck L et al (2015) Colorectal cancer screening: a global overview of existing programmes. Gut 64(10):1637–1649. https://doi.org/10.1136/gutjnl-2014-309086 CrossRefPubMed

40.

Levin TR, Jamieson L, Burley DA, Reyes J, Oehrli M, Caldwell C (2011) Organized colorectal cancer screening in integrated health care systems. Epidemiol Rev 33(1):101–110. https://doi.org/10.1093/epirev/mxr007 CrossRefPubMed

41.

Redelmeier DA, Tan SH, Booth GL (1998) The treatment of unrelated disorders in patients with chronic medical diseases. N Engl J Med 338(21):1516–1520. https://doi.org/10.1056/NEJM199805213382106 CrossRefPubMed

42.

Grant RW, Pirraglia PA, Melgs JB, Singer DE (2004) Trends in complexity of diabetes care in the United States from 1991 to 2000. Arch Intern Med 164(10):1134–1139. https://doi.org/10.1001/archinte.164.10.1134 CrossRefPubMed

43.

Sinnott C, Mc Hugh S, Browne J, Bradley C (2013) GPs’ perspectives on the management of patients with multimorbidity: systematic review and synthesis of qualitative research. BMJ Open 3(9):e003610. https://doi.org/10.1136/bmjopen-2013-003610 CrossRefPubMedPubMedCentral

44.

Jaen CR, Stange KC, Nutting PA (1994) Competing demands of primary care: a model for the delivery of clinical preventive services. J Fam Pract 38(2):166–174PubMed

45.

Decker SL, Burt CW, Sisk JE (2009) Trends in diabetes treatment patterns among primary care providers. J Ambulatory Care Manage 32(4):333–341. https://doi.org/10.1097/JAC.0b013e3181ba6e9e CrossRefPubMed

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):42–45

47.

Grady KE, Lemkau JP, McVay JM, Reisine ST (1992) The importance of physician encouragement in breast cancer screening of older women. Prev Med 21(6):766–780. https://doi.org/10.1016/0091-7435(92)90083-T CrossRefPubMed

48.

Moher D, Liberati A, Tetzlaff J, Altman DG, for the PRISMA group (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ 339:b2535. https://doi.org/10.1136/bmj.b2535 CrossRefPubMedPubMedCentral

49.

Liberati A, Altman DG, Tetzlaff J et al (2009) The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ 339:b2700. https://doi.org/10.1136/bmj.b2700 CrossRefPubMedPubMedCentral

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

51.

Shamseer L, Moher D, Clarke M et al (2015) Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: elaboration and explanation. BMJ 349:g7647. https://doi.org/10.1136/bmj.g7647 CrossRef

52.

Moher D, Stewart L, Shekelle P (2016) Implementing PRISMA-P: recommendations for prospective authors. Syst Rev 5(1):15. https://doi.org/10.1186/s13643-016-0191-y CrossRefPubMedPubMedCentral

53.

Terret C, Castel-Kremer E, Albrand G, Droz JP (2009) Effects of comorbidity on screening and early diagnosis of cancer in elderly people. Lancet Oncol 10(1):80–87. https://doi.org/10.1016/S1470-2045(08)70336-X CrossRefPubMed

54.

Wools A, Dapper EA, de Leeuw JRJ (2016) Colorectal cancer screening participation: a systematic review. Eur J Pub Health 26(1):158–168. https://doi.org/10.1093/eurpub/ckv148 CrossRef

55.

Diaz A, Kang J, Moore SP et al (2017) Association between comorbidity and participation in breast and cervical cancer screening: a systematic review and meta-analysis. Cancer Epidemiol 47:7–19. https://doi.org/10.1016/j.canep.2016.12.010 CrossRefPubMed

56.

Bramer WM, Giustini D, de Jonge GB, Holland L, Bekhuis T (2016) De-duplication of database search results for systematic reviews in EndNote. J Med Libr Assoc 104(3):240–243. https://doi.org/10.3163/1536-5050.104.3.014 CrossRefPubMedPubMedCentral

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

59.

Greiner KA, Daley CM, Epp A, James A, Yeh H-W, Geana M et al (2014) Implementation intentions and colorectal screening. Am J Prev Med 47(6):703–714. https://doi.org/10.1016/j.amepre.2014.08.005 CrossRefPubMedPubMedCentral

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

61.

DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7(3):177–188. https://doi.org/10.1016/0197-2456(86)90046-2 CrossRefPubMed

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

63.

Tamhane AR, Westfall AO, Burkholder GA, Cutter GR (2016) Prevalence odds ratio versus prevalence ratio: choice comes with consequences: prevalence odds ratio versus prevalence ratio. Stat Med 35(30):5730–5735. https://doi.org/10.1002/sim.7059 CrossRefPubMedPubMedCentral

64.

Thompson ML, Myers JE, Kriebel D (1998) Prevalence odds ratio or prevalence ratio in the analysis of cross sectional data: what is to be done? Occup Environ Med 55(4):272–277. https://doi.org/10.1136/oem.55.4.272 CrossRefPubMedPubMedCentral

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

66.

Miller EA, Tarasenko YN, Parker JD, Schoendorf KC (2014) Diabetes and colorectal cancer screening among men and women in the USA: National Health Interview Survey: 2008, 2010. Cancer Causes Control 25(5):553–560. https://doi.org/10.1007/s10552-014-0360-z CrossRefPubMed

67.

Dickersin K (2002) Systematic reviews in epidemiology: why are we so far behind? Int J Epidemiol 31(1):6–12. https://doi.org/10.1093/ije/31.1.6 CrossRefPubMed

68.

Egger M, Schneider M, Smith GD (1998) Meta-analysis spurious precision? Meta-analysis of observational studies. BMJ 316(7125):140–144. https://doi.org/10.1136/bmj.316.7125.140 CrossRefPubMedPubMedCentral

69.

Cummings P (2009) The relative merits of risk ratios and odds ratios. Arch Pediatr Adolesc Med 163(5):438. https://doi.org/10.1001/archpediatrics.2009.31 CrossRefPubMed

70.

Oluyemi AO, Welch AR, Yoo LJ, Lehman EB, McGarrity TJ, Chuang CH (2014) Colorectal cancer screening in high-risk groups is increasing, although current smokers fall behind: CRC screening in high-risk groups. Cancer 120(14):2106–2113. https://doi.org/10.1002/cncr.28707 CrossRefPubMed

71.

Beckman TJ, Cuddihy RM, Scheitel SM, Naessens JM, Killian JM, Pankratz VS (2001) Screening mammogram utilization in women with diabetes. Diabetes Care 24(12):2049–2053. https://doi.org/10.2337/diacare.24.12.2049 CrossRefPubMed

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 CrossRefPubMed

73.

Chan W, Yun L, Austin PC et al (2014) Impact of socio-economic status on breast cancer screening in women with diabetes: a population-based study. Diabet Med 31(7):806–812. https://doi.org/10.1111/dme.12422 CrossRefPubMed

74.

Katz D, Tengekyon AJ, Kahan NR, Calderon-Margalit R (2018) Patient and physician characteristics affect adherence to screening mammography: a population-based cohort study. PLoS One.13(3):e0194409, https://doi.org/10.1371/journal.pone.0194409 CrossRefPubMedPubMedCentral

75.

Lipscombe LL, Hux JE, Booth GL (2005) Reduced screening mammography among women with diabetes. Arch Intern Med 165(18):2090–2095. https://doi.org/10.1001/archinte.165.18.2090 CrossRefPubMed

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

77.

El Bcheraoui C, Basulaiman M, Wilson S, et al. (2015) Breast cancer screening in Saudi Arabia: free but almost no takers. PLoS One: 10(3):e0119051. https://doi.org/10.1371/journal.pone.0119051 CrossRefPubMedPubMedCentral

78.

Sanderson M, Lipworth L, Han X et al (2014) Mammography use among women with and without diabetes: results from the southern community cohort study. J Epidemiol Glob Health 4(3):223–230. https://doi.org/10.1016/j.jegh.2014.03.001 CrossRefPubMedPubMedCentral

79.

Abdullah NN, Daud S, Al-Kubaisy W, Saari IS, Saad SR (2016) Cervical cancer screening after 50: near extinction? Eur J Obstet Gynecol Reprod Biol 206:136–140. https://doi.org/10.1016/j.ejogrb.2016.09.011 CrossRefPubMed

80.

Richard A, Rohrmann S, Schmid SM et al (2015) Lifestyle and health-related predictors of cervical cancer screening attendance in a Swiss population-based study. Cancer Epidemiol 39(6):870–876. https://doi.org/10.1016/j.canep.2015.09.009 CrossRefPubMed

81.

Wernli KJ, Hubbard RA, Johnson E et al (2014) Patterns of colorectal cancer screening uptake in newly eligible men and women. Cancer Epidemiol Biomark Prev 23(7):1230–1237. https://doi.org/10.1158/1055-9965.EPI-13-1360 CrossRef

82.

Brittain K, Murphy VP (2015) Sociocultural and health correlates related to colorectal cancer screening adherence among urban African Americans. Cancer Nurs 38(2):118–124. https://doi.org/10.1097/NCC.0000000000000157 CrossRefPubMedPubMedCentral

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

84.

Singh H, Bernstein CN, Samadder JN, Ahmed R (2015) Screening rates for colorectal cancer in Canada: a cross-sectional study. CMAJ Open 3(2):E149–E157. https://doi.org/10.9778/cmajo.20140073 CrossRefPubMedPubMedCentral

85.

Bell RA, Shelton BJ, Paskett ED (2001) Colorectal cancer screening in North Carolina: associations with diabetes mellitus and demographic and health characteristics. Prev Med 32(2):163–167. https://doi.org/10.1006/pmed.2000.0785 CrossRefPubMed

86.

Kiefe CI, Funkhouser E, Fouad MN, May DS (1998) Chronic disease as a barrier to breast and cervical cancer screening. J Gen Intern Med 13(6):357–365. https://doi.org/10.1046/j.1525-1497.1998.00115.x CrossRefPubMedPubMedCentral

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 CrossRefPubMedPubMedCentral

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):1–15

90.

Marshall JG, Cowell JM, Campbell ES, McNaughton DB (2010) Regional variations in cancer screening rates found in women with diabetes. Nurs Res 59(1):34–41. https://doi.org/10.1097/NNR.0b013e3181c3bd07 CrossRefPubMed

91.

López-de-Andrés A, Martin-Lopez R, Hernández-Barrera V et al (2010) Predictors of breast and cervical cancer screening in a Spanish metropolitan area. J Women’s Health 19(9):1675–1681. https://doi.org/10.1089/jwh.2009.1828 CrossRef

92.

Jimenez-Garcia R, Hernandez-Barrera V, Carrasco-Garrido P, Gil A (2009) Prevalence and predictors of breast and cervical cancer screening among Spanish women with diabetes. Diabetes Care 32(8):1470–1472. https://doi.org/10.2337/dc09-0479 CrossRefPubMedPubMedCentral

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 CrossRefPubMed

94.

McBean AM, Yu X (2007) The underuse of screening services among elderly women with diabetes. Diabetes Care 30(6):1466–1472. https://doi.org/10.2337/dc06-2233 CrossRefPubMed

95.

Heflin MT, Oddone EZ, Pieper CF, Burchett BM, Cohen HJ (2002) The effect of comorbid illness on receipt of cancer screening by older people. J Am Geriatr Soc 50(10):1651–1658. https://doi.org/10.1046/j.1532-5415.2002.50456.x CrossRefPubMed

96.

Fleming ST, Love MM, Bennett K (2011) Diabetes and cancer screening rates among Appalachian and non-Appalachian residents of Kentucky. J Am Board Fam Med 24(6):682–692. https://doi.org/10.3122/jabfm.2011.06.110094 CrossRefPubMed

97.

Fontana SA, Baumann LC, Helberg C, Love RR (1997) The delivery of preventive services in primary care practices according to chronic disease status. Am J Public Health 87(7):1190–1196. https://doi.org/10.2105/AJPH.87.7.1190 CrossRefPubMedPubMedCentral

98.

Hsia J, Kemper E, Kiefe C et al (2000) The importance of health insurance as a determinant of cancer screening: evidence from the Women’s Health Initiative. Prev Med 31(3):261–270. https://doi.org/10.1006/pmed.2000.0697 CrossRefPubMed

99.

Jimenez-Trujillo I, Jiménez-García R, Esteban-Hernández J et al (2015) Predictors of adherence to multiple clinical preventive recommendations among adults with diabetes in Spain. PLoS One 10(6):e0131844. https://doi.org/10.1371/journal.pone.0131844 CrossRefPubMedPubMedCentral

100.

Karathanasi I, Kamposioras K, Cortinovis I et al (2009) Moving ahead in diabetics’ cancer screening; food for thought from the Hellenic experience. Eur J Cancer Care (Engl) 18(3):255–263. https://doi.org/10.1111/j.1365-2354.2007.00858.x CrossRef

101.

Liu BY, O’Malley J, Mori M et al (2014) The association of type and number of chronic diseases with breast, cervical, and colorectal cancer screening. J Am Board Fam Med 27(5):669–681. https://doi.org/10.3122/jabfm.2014.05.140005 CrossRefPubMedPubMedCentral

102.

Owens MD, Beckles GLA, Ho KK-Y, Gorrell P, Brady J, Kaftarian JS (2008) Women with diagnosed diabetes across the life stages: underuse of recommended preventive care services. J Women’s Health 17(9):1415–1423. https://doi.org/10.1089/jwh.2008.1125 CrossRef

103.

Zhao G, Ford ES, Ahluwalia IB, Li C, Mokdad AH (2009) Prevalence and trends of receipt of cancer screenings among US women with diagnosed diabetes. J Gen Intern Med 24(2):270–275. https://doi.org/10.1007/s11606-008-0858-8 CrossRefPubMed

104.

Yuan X, Liu T, Wu L, Zou Z-Y, Li C. Validity of self-reported diabetes among middle-aged and older Chinese adults: the China health and retirement longitudinal study. BMJ Open 2015;5(4):e006633–e006633, https://doi.org/10.1136/bmjopen-2014-006633 CrossRefPubMedPubMedCentral

105.

Pastorino S, Richards M, Hardy R et al (2015) Validation of self-reported diagnosis of diabetes in the 1946 British birth cohort. Prim Care Diabetes 9(5):397–400. https://doi.org/10.1016/j.pcd.2014.05.003 CrossRefPubMedPubMedCentral

106.

Espelt A, Goday A, Franch J, Borrell C (2012) Validity of self-reported diabetes in health interview surveys for measuring social inequalities in the prevalence of diabetes: Table 1. J Epidemiol Community Health 66(7):e15–e15. https://doi.org/10.1136/jech.2010.112698 CrossRefPubMed

107.

Martin LM, Leff M, Calonge N, Garrett C, Nelson DE (2000) Validation of self-reported chronic conditions and health services in a managed care population. Am J Prev Med 18(3):215–218. https://doi.org/10.1016/S0749-3797(99)00158-0 CrossRefPubMed

108.

Schneider ALC, Pankow JS, Heiss G, Selvin E (2012) Validity and reliability of self-reported diabetes in the atherosclerosis risk in communities study. Am J Epidemiol 176(8):738–743. https://doi.org/10.1093/aje/kws156 CrossRefPubMedPubMedCentral

109.

Howard M, Agarwal G, Lytwyn A (2009) Accuracy of self-reports of Pap and mammography screening compared to medical record: a meta-analysis. Cancer Causes Control 20(1):1–13. https://doi.org/10.1007/s10552-008-9228-4 CrossRefPubMed

110.

Ferrante JM, Ohman-Strickland P, Hahn KA et al (2008) Self-report versus medical records for assessing cancer-preventive services delivery. Cancer Epidemiol Biomark Prev 17(11):2987–2994. https://doi.org/10.1158/1055-9965.EPI-08-0177 CrossRef

111.

Gordon NP, Hiatt RA, Lampert DI (1993) Concordance of self-reported data and medical record audit for six cancer screening procedures. J Natl Cancer Inst 85(7):566–570. https://doi.org/10.1093/jnci/85.7.566 CrossRefPubMed

112.

Lysy Z, Booth GL, Shah BR, Austin PC, Luo J, Lipscombe LL (2013) The impact of income on the incidence of diabetes: a population-based study. Diabetes Res Clin Pract 99(3):372–379. https://doi.org/10.1016/j.diabres.2012.12.005 CrossRefPubMed

113.

Singh SM, Paszat LF, Li C, He J, Vinden C, Rabeneck L (2004) Association of socioeconomic status and receipt of colorectal cancer investigations: a population-based retrospective cohort study. Can Med Assoc J 171(5):461–465. https://doi.org/10.1503/cmaj.1031921 CrossRef

114.

Eckstrom E, Feeny DH, Walter LC, Perdue LA, Whitlock EP (2013) Individualizing cancer screening in older adults: a narrative review and framework for future research. J Gen Intern Med 28(2):292–298. https://doi.org/10.1007/s11606-012-2227-x CrossRefPubMed

115.

Sterne JAC, Sutton AJ, Ioannidis JPA et al (2011) Recommendations for examining and interpreting funnel plot asymmetry in meta-analyses of randomised controlled trials. BMJ 343:d4002. https://doi.org/10.1136/bmj.d4002 CrossRefPubMed

116.

Morrison A, Polisena J, Husereau D et al (2012) The effect of English-language restriction on systematic review-based meta-analyses: a systematic review of empirical studies. Int J Technol Assess Health Care 28(02):138–144. https://doi.org/10.1017/S0266462312000086 CrossRefPubMed

117.

Taksler GB, Pfoh ER, Stange KC, Rothberg MB (2018) Association between number of preventive care guidelines and preventive care utilization by patients. Am J Prev Med 55(1):1–10. https://doi.org/10.1016/j.amepre.2018.03.011 CrossRefPubMedPubMedCentral

118.

Ostbye T, Yarnall KS, Krause KM, Pollak KI, Gradison M, Michener JL (2005) Is there time for management of patients with chronic diseases in primary care? Ann Fam Med 3(3):209–214. https://doi.org/10.1370/afm.310 CrossRefPubMedPubMedCentral

119.

Streja DA, Rabkin SW (1999) Factors associated with implementation of preventive care measures in patients with diabetes mellitus. Arch Intern Med 159(3):294–302. https://doi.org/10.1001/archinte.159.3.294 CrossRefPubMed

120.

Cheung A, Stukel TA, Alter DA et al (2017) Primary care physician volume and quality of diabetes care: a population-based cohort study. Ann Intern Med 166(4):240. https://doi.org/10.7326/M16-1056 CrossRefPubMed

121.

Ioannou GN, Chapko MK, Dominitz JA (2003) Predictors of colorectal cancer screening participation in the United States. Am J Gastroenterol 98(9):2082–2091. https://doi.org/10.1111/j.1572-0241.2003.07574.x CrossRefPubMed

122.

Gancayco J, Soulos PR, Khiani V et al (2013) Age-based and sex-based disparities in screening colonoscopy use among Medicare beneficiaries. J Clin Gastroenterol 47(7):630–636. https://doi.org/10.1097/MCG.0b013e31828345c8 CrossRefPubMed

123.

Klabunde C, Blom J, Bulliard J-L et al (2015) Participation rates for organized colorectal cancer screening programmes: an international comparison. J Med Screen 22(3):119–126. https://doi.org/10.1177/0969141315584694 CrossRefPubMed

124.

Sabatino SA, Lawrence B, Elder R et al (2012) Effectiveness of interventions to increase screening for breast, cervical, and colorectal cancers. Am J Prev Med 43(1):97–118. https://doi.org/10.1016/j.amepre.2012.04.009 CrossRefPubMed

125.

Duffy SW, Myles JP, Maroni R, Mohammad A (2017) Rapid review of evaluation of interventions to improve participation in cancer screening services. J Med Screen 24(3):127–145. https://doi.org/10.1177/0969141316664757 CrossRefPubMed

126.

van Rossum LG, van Rijn AF, Laheij RJ et al (2008) Random comparison of Guaiac and immunochemical fecal occult blood tests for colorectal cancer in a screening population. Gastroenterology 135(1):82–90. https://doi.org/10.1053/j.gastro.2008.03.040 CrossRefPubMed

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMed

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:i4924

130.

Nelson EJ, Maynard BR, Loux T, Fatla J, Gordon R, Arnold LD (2017) The acceptability of self-sampled screening for HPV DNA: a systematic review and meta-analysis. Sex Transm Infect 93(1):56–61. https://doi.org/10.1136/sextrans-2016-052609 CrossRefPubMed

131.

Rees I, Jones D, Chen H, Macleod U (2018) Interventions to improve the uptake of cervical cancer screening among lower socioeconomic groups: a systematic review. Prev Med 111:323–335. https://doi.org/10.1016/j.ypmed.2017.11.019 CrossRefPubMed

132.

Beeker C, Kraft JM, Southwell BG, Jorgensen CM (2000) Colorectal cancer screening in older men and women: qualitative research findings and implications for intervention. J Community Health 25(3):263–278. https://doi.org/10.1023/A:1005104406934 CrossRefPubMed

133.

Friedemann-Sánchez G, Griffin JM, Partin MR (2007) Gender differences in colorectal cancer screening barriers and information needs. Health Expect 10(2):148–160. https://doi.org/10.1111/j.1369-7625.2006.00430.x CrossRefPubMedPubMedCentral

134.

Elston Lafata J, Martin S, Morlock R, Divine G, Xi H (2001) Provider type and the receipt of general and diabetes-related preventive health services among patients with diabetes. Med Care 39(5):491–499. https://doi.org/10.1097/00005650-200105000-00009 CrossRef

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

136.

Nayor J, Maniar S, Chan WW (2017) Appointment-keeping behaviors and procedure day are associated with colonoscopy attendance in a patient navigator population. Prev Med 97:8–12. https://doi.org/10.1016/j.ypmed.2016.12.022 CrossRefPubMed

Title: Breast, cervical and colorectal cancer screening in adults with diabetes: a systematic review and meta-analysis
Authors: Dominika Bhatia
Iliana C. Lega
Wei Wu
Lorraine L. Lipscombe
Publication date: 01-01-2020
Publisher: Springer Berlin Heidelberg
Keywords: Breast Cancer
Cervical Cancer
Breast Cancer
Cervical Cancer
Colorectal Cancer
Colorectal Cancer
Published in: Diabetologia / Issue 1/2020
Print ISSN: 0012-186X
Electronic ISSN: 1432-0428
DOI: https://doi.org/10.1007/s00125-019-04995-7

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