Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Population-based screening for cancer: hope and hype

Key Points

  • Tumours within any organ site can have a spectrum of biological phenotypes, ranging from indolent to highly aggressive

  • Screening for cancer is most likely to be beneficial when the target tumour type has a relatively uniform biology and a slower rate of progression

  • Not all precursor lesions are on an obligate pathway towards invasive-cancer development

  • Strategies for early detection of cancer must balance the benefits of mortality reduction (and reduction in invasive-disease incidence with screening for precancers) with the heterogeneity of the target disease and the consequent risk of overdiagnosis

  • Screening can be viewed as a 'cascade' involving multiple steps, such as selection of individuals to be screened, administration of the screening test, workup of positive findings, and, ultimately, treatment

  • Efforts are underway to individualize decision-making surrounding risk stratification, the modality and frequency of screening, and diagnostic and therapeutic interventions tailored to the biology of the detected tumour

Abstract

Several important lessons have been learnt from our experiences in screening for various cancers. Screening programmes for cervical and colorectal cancers have had the greatest success, probably because these cancers are relatively homogenous, slow-growing, and have identifiable precursors that can be detected and removed; however, identifying the true obligate precursors of invasive disease remains a challenge. With regard to screening for breast cancer and for prostate cancer, which focus on early detection of invasive cancer, preferential detection of slower-growing, localized cancers has occurred, which has led to concerns about overdiagnosis and overtreatment; programmes for early detection of invasive lung cancers are emerging, and have faced similar challenges. A crucial consideration in screening for breast, prostate, and lung cancers is their remarkable phenotypic heterogeneity, ranging from indolent to highly aggressive. Efforts have been made to address the limitations of cancer-screening programmes, providing an opportunity for cross-disciplinary learning and further advancement of the science. Current innovations are aimed at identifying the individuals who are most likely to benefit from screening, increasing the yield of consequential cancers on screening and biopsy, and using molecular tests to improve our understanding of disease biology and to tailor treatment. We discuss each of these concepts and outline a dynamic framework for continuous improvements in the field of cancer screening.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Age-adjusted incidence rates of invasive cancers for which population-based screening is practiced in the USA.
Figure 2: A framework for ongoing improvement of cancer-screening programmes.

Similar content being viewed by others

References

  1. Wilson, J. M. & Jungner, Y. G. Principles and practice of screening for disease. Public Health Pap. 34, 1–163 (1968).

    Google Scholar 

  2. Vogelstein, B. et al. Genetic alterations during colorectal-tumor development. N. Engl. J. Med. 319, 525–532 (1988).

    Article  CAS  PubMed  Google Scholar 

  3. Gyorffy, B. et al. Multigene prognostic tests in breast cancer: past, present, future. Breast Cancer Res. 17, 11 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  4. National Cancer Institute. U.S. population data — 1969–2013. [online], (2015).

  5. Bleyer, A. & Welch, H. G. Effect of three decades of screening mammography on breast-cancer incidence. N. Engl. J. Med. 367, 1998–2005 (2012).

    Article  CAS  PubMed  Google Scholar 

  6. Worni, M. et al. Trends in treatment patterns and outcomes for ductal carcinoma in situ. J. Natl Cancer Inst. 107, djv263 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  7. Esserman, L., Shieh, Y. & Thompson, I. Rethinking screening for breast cancer and prostate cancer. JAMA 302, 1685–1692 (2009).

    Article  CAS  PubMed  Google Scholar 

  8. Welch, H. G., Gorski, D. H. & Albertsen, P. C. Trends in metastatic breast and prostate cancer — lessons in cancer dynamics. N. Engl. J. Med. 373, 1685–1687 (2015).

    Article  PubMed  Google Scholar 

  9. Kirsh, V. A. et al. Tumor characteristics associated with mammographic detection of breast cancer in the Ontario breast screening program. J. Natl Cancer Inst. 103, 942–950 (2011).

    Article  PubMed  Google Scholar 

  10. Shen, Y. et al. Role of detection method in predicting breast cancer survival: analysis of randomized screening trials. J. Natl Cancer Inst. 97, 1195–1203 (2005).

    Article  PubMed  Google Scholar 

  11. Woods, W. G. et al. Screening of infants and mortality due to neuroblastoma. N. Engl. J. Med. 346, 1041–1046 (2002).

    Article  PubMed  Google Scholar 

  12. Ahn, H. S., Kim, H. J. & Welch, H. G. Korea's thyroid-cancer 'epidemic' — screening and overdiagnosis. N. Engl. J. Med. 371, 1765–1767 (2014).

    Article  PubMed  Google Scholar 

  13. Siegel, R. L., Miller, K. D. & Jemal, A. Cancer statistics, 2016. CA Cancer J. Clin. 66, 7–30 (2016).

    Article  PubMed  Google Scholar 

  14. O'Grady, T. J., Gates, M. A. & Boscoe, F. P. Thyroid cancer incidence attributable to overdiagnosis in the United States 1981–2011. Int. J. Cancer 137, 2664–2673 (2015).

    Article  CAS  PubMed  Google Scholar 

  15. Peirson, L., Fitzpatrick-Lewis, D., Ciliska, D. & Warren, R. Screening for cervical cancer: a systematic review and meta-analysis. Syst. Rev. 2, 35 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  16. Whitlock, E. P. et al. Liquid-based cytology and human papillomavirus testing to screen for cervical cancer: a systematic review for the U.S. Preventive Services Task Force. Ann. Intern. Med. 155, 687–697 (2011).

    Article  PubMed  Google Scholar 

  17. Sankaranarayanan, R. et al. Effect of visual screening on cervical cancer incidence and mortality in Tamil Nadu, India: a cluster-randomised trial. Lancet 370, 398–406 (2007).

    Article  PubMed  Google Scholar 

  18. Sankaranarayanan, R. et al. HPV screening for cervical cancer in rural India. N. Engl. J. Med. 360, 1385–1394 (2009).

    Article  CAS  PubMed  Google Scholar 

  19. Shastri, S. S. et al. Effect of VIA screening by primary health workers: randomized controlled study in Mumbai, India. J. Natl Cancer Inst. 106, dju009 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  20. Andrae, B. et al. Screening-preventable cervical cancer risks: evidence from a nationwide audit in Sweden. J. Natl Cancer Inst. 100, 622–629 (2008).

    Article  PubMed  Google Scholar 

  21. National Institute of Health. Cervical cancer. NIH Consensus Statement. NIH Consensus Development Program [online], (1996).

  22. Rositch, A. F., Nowak, R. G. & Gravitt, P. E. Increased age and race-specific incidence of cervical cancer after correction for hysterectomy prevalence in the United States from 2000 to 2009. Cancer 120, 2032–2038 (2014).

    Article  PubMed  Google Scholar 

  23. Nishihara, R. et al. Long-term colorectal-cancer incidence and mortality after lower endoscopy. N. Engl. J. Med. 369, 1095–1105 (2013).

    Article  CAS  PubMed  Google Scholar 

  24. Brenner, H., Chang-Claude, J., Seiler, C. M., Rickert, A. & Hoffmeister, M. Protection from colorectal cancer after colonoscopy: a population-based, case–control study. Ann. Intern. Med. 154, 22–30 (2011).

    Article  PubMed  Google Scholar 

  25. Brenner, H., Stock, C. & Hoffmeister, M. Effect of screening sigmoidoscopy and screening colonoscopy on colorectal cancer incidence and mortality: systematic review and meta-analysis of randomised controlled trials and observational studies. BMJ 348, g2467 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  26. Weinberg, D. S. & Schoen, R. E. Screening for colorectal cancer. Ann. Intern. Med. 160, ITC5-1 (2014).

    Article  Google Scholar 

  27. Lieberman, D. A. et al. Use of colonoscopy to screen asymptomatic adults for colorectal cancer. Veterans Affairs Cooperative Study Group 380. N. Engl. J. Med. 343, 162–168 (2000).

    Article  CAS  PubMed  Google Scholar 

  28. Imperiale, T. F. et al. Risk of advanced proximal neoplasms in asymptomatic adults according to the distal colorectal findings. N. Engl. J. Med. 343, 169–174 (2000).

    Article  CAS  PubMed  Google Scholar 

  29. Rex, D. K. Colonoscopy: the current king of the hill in the USA. Dig. Dis. Sci. 60, 639–646 (2015).

    Article  PubMed  Google Scholar 

  30. United States Preventive Services Task Force. Screening for colorectal cancer: U.S. Preventive Services Task Force recommendation statement. Ann. Intern. Med. 149, 627–637 (2008).

  31. Zauber, A. G. The impact of screening on colorectal cancer mortality and incidence: has it really made a difference? Dig. Dis. Sci. 60, 681–691 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  32. Moyer, V. A. Screening for cervical cancer: U.S. Preventive Services Task Force recommendation statement. Ann. Intern. Med. 156, 880–891 (2012).

    Article  PubMed  Google Scholar 

  33. Vesco, K. K. et al. Screening for Cervical Cancer: A Systematic Evidence Review for the U.S. Preventive Services Task Force (Agency for Healthcare Research and Quality, 2011).

  34. Grady, W. M. & Markowitz, S. D. The molecular pathogenesis of colorectal cancer and its potential application to colorectal cancer screening. Dig. Dis. Sci. 60, 762–772 (2015).

    Article  CAS  PubMed  Google Scholar 

  35. ASCUS-LSIL Triage Study (ALTS) Group. Results of a randomized trial on the management of cytology interpretations of atypical squamous cells of undetermined significance. Am. J. Obstet. Gynecol. 188, 1383–1392 (2003).

  36. Pickhardt, P. J. et al. Assessment of volumetric growth rates of small colorectal polyps with CT colonography: a longitudinal study of natural history. Lancet Oncol. 14, 711–720 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  37. Levin, T. R. et al. Complications of colonoscopy in an integrated health care delivery system. Ann. Intern. Med. 145, 880–886 (2006).

    Article  PubMed  Google Scholar 

  38. Ko, C. W. et al. Incidence of minor complications and time lost from normal activities after screening or surveillance colonoscopy. Gastrointest. Endosc. 65, 648–656 (2007).

    Article  PubMed  Google Scholar 

  39. Kyrgiou, M. et al. Fertility and early pregnancy outcomes after conservative treatment for cervical intraepithelial neoplasia. Cochrane Database Syst. Rev. 9, CD008478 (2015).

    Google Scholar 

  40. Conner, S. N. et al. Loop electrosurgical excision procedure and risk of preterm birth: a systematic review and meta-analysis. Obstet. Gynecol. 123, 752–761 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  41. Ernster, V. L., Barclay, J., Kerlikowske, K., Grady, D. & Henderson, C. Incidence of and treatment for ductal carcinoma in situ of the breast. JAMA 275, 913–918 (1996).

    Article  CAS  PubMed  Google Scholar 

  42. Ozanne, E. et al. Characterizing the impact of 25 years of DCIS treatment. Breast Cancer Res. Treat. 129, 165–173 (2011).

    Article  PubMed  Google Scholar 

  43. Baxter, N. N., Virnig, B. A., Durham, S. B. & Tuttle, T. M. Trends in the treatment of ductal carcinoma in situ of the breast. J. Natl Cancer Inst. 96, 443–448 (2004).

    Article  PubMed  Google Scholar 

  44. Narod, S. A., Iqbal, J., Giannakeas, V., Sopik, V. & Sun, P. Breast cancer mortality after a diagnosis of ductal carcinoma in situ. JAMA Oncol. 1, 888–896 (2015).

    Article  PubMed  Google Scholar 

  45. Solin, L. J. et al. A multigene expression assay to predict local recurrence risk for ductal carcinoma in situ of the breast. J. Natl Cancer Inst. 105, 701–710 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. Sanders, M. E. et al. Continued observation of the natural history of low-grade ductal carcinoma in situ reaffirms proclivity for local recurrence even after more than 30 years of follow-up. Modern Pathol. 28, 662–669 (2014).

    Article  Google Scholar 

  47. Leonard, G. D. & Swain, S. M. Ductal carcinoma in situ, complexities and challenges. J. Natl Cancer Inst. 96, 901–920 (2004).

    Article  Google Scholar 

  48. Sagara, Y. et al. Survival benefit of breast surgery for low-grade ductal carcinoma in situ: a population-based cohort study. JAMA Surg. 150, 739–745 (2015).

    Article  PubMed  Google Scholar 

  49. Bijker, N. et al. Risk factors for recurrence and metastasis after breast-conserving therapy for ductal carcinoma-in-situ: analysis of European Organization for Research and Treatment of Cancer Trial 10853. J. Clin. Oncol. 19, 2263–2271 (2001).

    Article  CAS  PubMed  Google Scholar 

  50. Fisher, E. R. et al. Pathologic findings from the National Surgical Adjuvant Breast Project (NSABP) eight-year update of Protocol B-17: intraductal carcinoma. Cancer 86, 429–438 (1999).

    Article  CAS  PubMed  Google Scholar 

  51. Campbell, M. J., et al. Characterizing the tumor immune microenvironment (TIME) in high-risk ductal carcinoma in situ [abstract]. Cancer Res. 75, PD1-5 (2015).

    Google Scholar 

  52. Habbema, J. D., van Oortmarssen, G. J., van Putten, D. J., Lubbe, J. T. & van der Maas, P. J. Age-specific reduction in breast cancer mortality by screening: an analysis of the results of the Health Insurance Plan of Greater New York study. J. Natl Cancer Inst. 77, 317–320 (1986).

    CAS  PubMed  Google Scholar 

  53. Nystrom, L. et al. Long-term effects of mammography screening: updated overview of the Swedish randomised trials. Lancet 359, 909–919 (2002).

    Article  PubMed  Google Scholar 

  54. Tabar, L. et al. Efficacy of breast cancer screening by age. New results from the Swedish Two-County Trial. Cancer 75, 2507–2517 (1995).

    Article  CAS  PubMed  Google Scholar 

  55. Miller, A. B. et al. Twenty five year follow-up for breast cancer incidence and mortality of the Canadian National Breast Screening Study: randomised screening trial. BMJ 348, g366 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  56. Moss, S. M. et al. Effect of mammographic screening from age 40 years on breast cancer mortality in the UK Age trial at 17 years' follow-up: a randomised controlled trial. Lancet Oncol. 16, 1123–1132 (2015).

    Article  PubMed  Google Scholar 

  57. Gotzsche, P. C. & Jorgensen, K. J. Screening for breast cancer with mammography. Cochrane Database Syst. Rev. 6, CD001877 (2013).

    Google Scholar 

  58. Myers, E. R., Moorman, P., Gierisch, J. M., Havrilesky, L. J. & Grimm, L. J. Benefits and harms of breast cancer screening: a systematic review. JAMA 314, 1615–1634 (2015).

    Article  CAS  PubMed  Google Scholar 

  59. Nelson, H. D. et al. Effectiveness of breast cancer screening: systematic review and meta-analysis to update the 2009 U.S. Preventive Services Task Force Recommend. Ann. Intern. Med. 164, 244–255 (2016).

    Article  PubMed  Google Scholar 

  60. Birnbaum, J., Gadi, V. K. & Markowitz, E. The effect of treatment advances on the mortality results of breast cancer screening trials: a microsimulation model. Ann. Intern. Med. 164, 236–243 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  61. Berry, D. A. et al. Effect of screening and adjuvant therapy on mortality from breast cancer. N. Engl. J. Med. 353, 1784–1792 (2005).

    Article  CAS  PubMed  Google Scholar 

  62. Autier, P. Efficient treatments reduce the cost-efficiency of breast cancer screening. Ann. Intern. Med. 164, 297–308 (2016).

    Article  PubMed  Google Scholar 

  63. Welch, H. G. & Passow, H. J. Quantifying the benefits and harms of screening mammography. JAMA Intern. Med. 174, 448–454 (2014).

    Article  PubMed  Google Scholar 

  64. Harding, C. et al. Breast cancer screening, incidence, and mortality across US counties. JAMA Intern. Med. 175, 1483–1489 (2015).

    Article  PubMed  Google Scholar 

  65. Siu, A. L. Screening for breast cancer: U.S. Preventive Services Task Force recommendation statement. Ann Intern. Med. 164, 279–296 (2016).

    Article  PubMed  Google Scholar 

  66. Mandelblatt, J. S., Stout, N. K. & Schechter, C. B. Collaborative modeling of the benefits and harms associated with different U.S. breast cancer screening strategies. Ann. Intern. Med. 164, 215–225 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  67. Nelson, H. D., Pappas, M. & Cantor, A. Harms of breast cancer screening: systematic review to update the 2009 U.S. Preventive Services Task Force recommendation. Ann. Intern. Med. 164, 256–267 (2016).

    Article  PubMed  Google Scholar 

  68. Oeffinger, K. C. et al. Breast cancer screening for women at average risk: 2015 guideline update from the American Cancer Society. JAMA 314, 1599–1614 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  69. American College of Obstetricians–Gynecologists. Practice bulletin no. 122: breast cancer screening. Obstet.Gynecol. 118, 372–382 (2011).

  70. Mainiero, M. B. et al. ACR appropriateness criteria breast cancer screening. J. Am. Coll. Radiol. 10, 11–14 (2013).

    Article  PubMed  Google Scholar 

  71. Liston, J. & Wilson, R. (eds) Clinical guidelines for breast cancer screening assessment. GOV.UK [online], (2010).

    Google Scholar 

  72. de Jong, N., Lock, A., Carpay, M. & Hoebee, B. Dutch Breast Cancer Screening Program: organization and effectiveness. National Institute for Public Health and the Environment [online], (2014).

    Google Scholar 

  73. Socialstyrelsen. Screening för bröstcancer — rekommendation och bedömningsunderlag. [online], (2014).

  74. Etzioni, R. et al. The prostate cancer conundrum revisited: treatment changes and prostate cancer mortality declines. Cancer 118, 5955–5963 (2012).

    Article  PubMed  Google Scholar 

  75. Andriole, G. L. et al. Mortality results from a randomized prostate-cancer screening trial. N. Engl. J. Med. 360, 1310–1319 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  76. Schroder, F. H. et al. Screening and prostate-cancer mortality in a randomized European study. N. Engl. J. Med. 360, 1320–1328 (2009).

    Article  PubMed  Google Scholar 

  77. Schroder, F. H. & Roobol, M. J. ERSPC and PLCO prostate cancer screening studies: what are the differences? Eur. Urol. 58, 46–52 (2010).

    Article  PubMed  Google Scholar 

  78. Yin, M., Bastacky, S., Chandran, U., Becich, M. J. & Dhir, R. Prevalence of incidental prostate cancer in the general population: a study of healthy organ donors. J. Urol. 179, 892–895; discussion 895 (2008).

    Article  PubMed  Google Scholar 

  79. Thompson, I. M. et al. Prevalence of prostate cancer among men with a prostate-specific antigen level ≤4.0 ng per milliliter. N. Engl. J. Med. 350, 2239–2246 (2004).

    Article  CAS  PubMed  Google Scholar 

  80. Moyer, V. A. Screening for prostate cancer: U. S. Preventive Services Task Force recommendation statement. Ann. Intern. Med. 157, 120–134 (2012).

    Article  PubMed  Google Scholar 

  81. Arnsrud Godtman, R., Holmberg, E., Lilja, H., Stranne, J. & Hugosson, J. Opportunistic testing versus organized prostate-specific antigen screening: outcome after 18 years in the Goteborg randomized population-based prostate cancer screening trial. Eur. Urol. 68, 354–360 (2015).

    Article  PubMed  Google Scholar 

  82. Wolf, A. & Wender, R. C. American Cancer Society guideline for the early detection of prostate cancer: update 2010. CA Cancer J. Clin. 60, 70–98 (2015).

    Article  Google Scholar 

  83. Carter, H. B. et al. Early detection of prostate cancer: AUA guideline. J. Urol. 190, 419–426 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  84. Heidenreich, A. et al. EAU guidelines on prostate cancer. Part 1: screening, diagnosis, and local treatment with curative intent — update 2013. Eur. Urol. 65, 124–137 (2014).

    Article  PubMed  Google Scholar 

  85. National Lung Screening Trial Research Team. Results of initial low-dose computed tomographic screening for lung cancer. N. Engl. J. Med. 368, 1980–1991 (2013).

  86. Pinsky, P. F., Church, T. R., Izmirlian, G. & Kramer, B. S. The National Lung Screening Trial: results stratified by demographics, smoking history, and lung cancer histology. Cancer 119, 3976–3983 (2013).

    Article  PubMed  Google Scholar 

  87. Aberle, D. R. et al. Reduced lung-cancer mortality with low-dose computed tomographic screening. N. Engl. J. Med. 365, 395–409 (2011).

    Article  PubMed  Google Scholar 

  88. Patz, E. F. Jr et al. Overdiagnosis in low-dose computed tomography screening for lung cancer. JAMA Intern. Med. 174, 269–274 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  89. Pinsky, P. F. et al. Performance of Lung-RADS in the National Lung Screening Trial: a retrospective assessment. Ann. Intern. Med. 162, 485–491 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  90. Horeweg, N. et al. Detection of lung cancer through low-dose CT screening (NELSON): a prespecified analysis of screening test performance and interval cancers. Lancet Oncol. 15, 1342–1350 (2014).

    Article  PubMed  Google Scholar 

  91. Bach, P. B. et al. Benefits and harms of CT screening for lung cancer: a systematic review. JAMA 307, 2418–2429 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  92. Moyer, V. A. Screening for lung cancer: U.S. Preventive Services Task Force recommendation statement. Ann. Intern. Med. 160, 330–338 (2014).

    PubMed  Google Scholar 

  93. Wender, R. et al. American Cancer Society lung cancer screening guidelines. CA Cancer J. Clin. 63, 106–117 (2015).

    Article  Google Scholar 

  94. Tanoue, L. T., Tanner, N. T., Gould, M. K. & Silvestri, G. A. Lung cancer screening. Am. J. Respir. Crit. Care Med. 191, 19–33 (2015).

    Article  PubMed  Google Scholar 

  95. van 't Veer, L. J. et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature 415, 530–536 (2002).

    Article  CAS  PubMed  Google Scholar 

  96. Paik, S. et al. A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N. Engl. J. Med. 351, 2817–2826 (2004).

    Article  CAS  PubMed  Google Scholar 

  97. Sorlie, T. et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc. Natl Acad. Sci. USA 98, 10869–10874 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Woloshin, S., Schwartz, L. M., Black, W. C. & Kramer, B. S. Cancer screening campaigns — getting past uninformative persuasion. N. Engl. J. Med. 367, 1677–1679 (2012).

    Article  CAS  PubMed  Google Scholar 

  99. Wilt, T. J., Harris, R. P. & Qaseem, A. Screening for cancer: advice for high-value care from the American College of Physicians. Ann. Intern. Med. 162, 718–725 (2015).

    Article  PubMed  Google Scholar 

  100. Hoffman, T. C. & Del Mar, C. Patients' expectations of the benefits and harms of treatments, screening, and tests: a systematic review. JAMA Intern. Med. 175, 274–286 (2015).

    Article  Google Scholar 

  101. Moynihan, R. et al. Public opinions about overdiagnosis: a national community survey. PLoS ONE 10, e0125165 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  102. Prasad, V., Lenzer, J. & Newman, D. H. Why cancer screening has never been shown to 'save lives' — and what we can do about it. BMJ 352, h6080 (2016).

    Article  CAS  PubMed  Google Scholar 

  103. Smith-Bindman, R. et al. Comparison of screening mammography in the United States and the United Kingdom. JAMA 290, 2129–2137 (2003).

    Article  CAS  PubMed  Google Scholar 

  104. Kemp Jacobsen, K. et al. Comparing sensitivity and specificity of screening mammography in the United States and Denmark. Int. J. Cancer 137, 2198–2207 (2015).

    Article  CAS  PubMed  Google Scholar 

  105. Esserman, L. et al. Improving the accuracy of mammography: volume and outcome relationships. J. Natl Cancer Inst. 94, 369–375 (2002).

    Article  PubMed  Google Scholar 

  106. US Preventive Services Task Force. Screening for breast cancer: U.S. Preventive Services Task Force recommendation statement. Ann. Intern. Med. 151, 716–726 (2009).

  107. Esserman, L. J. et al. Addressing overdiagnosis and overtreatment in cancer: a prescription for change. Lancet Oncol. 15, e234–e242 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  108. Sawaya, G. F. et al. Cervical cancer screening in average-risk women: best practice advice from the Clinical Guidelines Committee of the American College of Physicians. Ann. Intern. Med. 162, 851–859 (2015).

    Article  PubMed  Google Scholar 

  109. Harris, R. P., Wilt, T. J. & Qaseem, A. A value framework for cancer screening: advice for high-value care from the American College of Physicians. Ann. Intern. Med. 162, 712–717 (2015).

    Article  PubMed  Google Scholar 

  110. Jorgensen, K. J. & Gotzsche, P. C. Breast cancer: updated screening guidelines — much ado about small improvements. Nat. Rev. Clin. Oncol. 13, 139–140 (2016).

    Article  PubMed  Google Scholar 

  111. Stoffel, E. M. et al. Hereditary colorectal cancer syndromes: American Society of Clinical Oncology Clinical Practice Guideline endorsement of the familial risk-colorectal cancer: European Society for Medical Oncology Clinical Practice Guidelines. J. Clin. Oncol. 33, 209–217 (2015).

    Article  PubMed  Google Scholar 

  112. Cairns, S. R. et al. Guidelines for colorectal cancer screening and surveillance in moderate and high risk groups (update from 2002). Gut 59, 666–689 (2010).

    Article  PubMed  Google Scholar 

  113. Kornbluth, A. & Sachar, D. B. Ulcerative colitis practice guidelines in adults: American College of Gastroenterology, Practice Parameters Committee. Am. J. Gastroenterol. 105, 501–523; quiz 524 (2010).

    Article  PubMed  Google Scholar 

  114. Ruparel, M. & Navani, N. Fulfilling the dream. Toward reducing inequalities in lung cancer screening. Am. J. Respir. Crit. Care Med. 192, 125–127 (2015).

    Article  PubMed  Google Scholar 

  115. Imperiale, T. F., Monahan, P. O., Stump, T. E., Glowinski, E. A. & Ransohoff, D. F. Derivation and validation of a scoring system to stratify risk for advanced colorectal neoplasia in asymptomatic adults: a cross-sectional study. Ann. Intern. Med. 163, 339–346 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  116. Tammemagi, M. C. et al. Selection criteria for lung-cancer screening. N. Engl. J. Med. 368, 728–736 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  117. Wright, T. C. et al. Primary cervical cancer screening with human papillomavirus: end of study results from the ATHENA study using HPV as the first-line screening test. Gynecol. Oncol. 136, 189–197 (2015).

    Article  PubMed  Google Scholar 

  118. Huh, W. K. et al. Use of primary high-risk human papillomavirus testing for cervical cancer screening: interim clinical guidance. Gynecol. Oncol. 136, 178–182 (2015).

    Article  PubMed  Google Scholar 

  119. Gail, M. H. et al. Projecting individualized probabilities of developing breast cancer for white females who are being examined annually. J. Natl Cancer Inst. 81, 1879–1886 (1989).

    Article  CAS  PubMed  Google Scholar 

  120. Tyrer, J., Duffy, S. W. & Cuzick, J. A breast cancer prediction model incorporating familial and personal risk factors. Stat. Med. 23, 1111–1130 (2004).

    Article  PubMed  Google Scholar 

  121. Mavaddat, N., Rebbeck, T. R., Lakhani, S. R., Easton, D. F. & Antoniou, A. C. Incorporating tumour pathology information into breast cancer risk prediction algorithms. Breast Cancer Res. 12, R28 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  122. Tice, J. A. et al. Using clinical factors and mammographic breast density to estimate breast cancer risk: development and validation of a new predictive model. Ann. Intern. Med. 148, 337–347 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  123. Tice, J. A. et al. Breast density and benign breast disease: risk assessment to identify women at high risk of breast cancer. J. Clin. Oncol. 33, 3137–3143 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  124. Saslow, D. et al. American Cancer Society guidelines for breast screening with MRI as an adjunct to mammography. CA Cancer J. Clin. 57, 75–89 (2007).

    Article  PubMed  Google Scholar 

  125. Vachon, C. M. et al. The contributions of breast density and common genetic variation to breast cancer risk. J. Natl Cancer Inst. 107, dju397 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  126. Michailidou, K. et al. Genome-wide association analysis of more than 120,000 individuals identifies 15 new susceptibility loci for breast cancer. Nat. Genet. 47, 373–380 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  127. Wisdom. About the study. [online], (2015).

  128. Schoots, I. G. et al. Magnetic resonance imaging-targeted biopsy may enhance the diagnostic accuracy of significant prostate cancer detection compared to standard transrectal ultrasound-guided biopsy: a systematic review and meta-analysis. Eur. Urol. 68, 438–450 (2015).

    Article  PubMed  Google Scholar 

  129. Warner, E. et al. Surveillance of BRCA1 and BRCA2 mutation carriers with magnetic resonance imaging, ultrasound, mammography, and clinical breast examination. JAMA 292, 1317–1325 (2004).

    Article  CAS  PubMed  Google Scholar 

  130. Kriege, M. et al. Efficacy of MRI and mammography for breast-cancer screening in women with a familial or genetic predisposition. N. Engl. J. Med. 351, 427–437 (2004).

    Article  CAS  PubMed  Google Scholar 

  131. Lee, C. H. et al. Breast cancer screening with imaging: recommendations from the Society of Breast Imaging and the ACR on the use of mammography, breast MRI, breast ultrasound, and other technologies for the detection of clinically occult breast cancer. J. Am. Coll. Radiol. 7, 18–27 (2010).

    Article  PubMed  Google Scholar 

  132. Lieberman, D. A. et al. Guidelines for colonoscopy surveillance after screening and polypectomy: a consensus update by the US Multi-Society Task Force on Colorectal Cancer. Gastroenterology 143, 844–857 (2012).

    Article  PubMed  Google Scholar 

  133. Kerlikowske, K. et al. Outcomes of screening mammography by frequency, breast density, and postmenopausal hormone therapy. JAMA Intern. Med. 173, 807–816 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  134. Grönberg, H. et al. Prostate cancer screening in men aged 50–69 years (STHLM3): a prospective population-based diagnostic study. Lancet Oncol. 16, 1667–1676 (2015).

    Article  PubMed  Google Scholar 

  135. Massad, L. S. et al. 2012 updated consensus guidelines for the management of abnormal cervical cancer screening tests and cancer precursors. Obstet. Gynecol. 121, 829–846 (2013).

    Article  PubMed  Google Scholar 

  136. American College of Radiology. Lung CT Screening Reporting and Data System (Lung-RADS). [online], (2015).

  137. Lindstrom, L. S. et al. MammaPrint accurately predicts long-term survival (25 years) and adjuvant tamoxifen therapy benefit in lymph node and negative patients (abstract). Cancer Res. 75 (Suppl. 9), P4-11-12 (2015).

    Google Scholar 

  138. Esserman, L. J. et al. Impact of mammographic screening on the detection of good and poor prognosis breast cancers. Breast Cancer Res. Treat. 130, 725–734 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  139. National Cancer Institute Division of Cancer Prevention. Consortium for Molecular Characterization of Screen-Detected Lesions Created: eight grants awarded. [online], (2015).

  140. Bennett, R. L., Blanks, R. G., Patnick, J. & Moss, S. M. Results from the UK NHS Breast Screening Programme 2000–2005. J. Med. Screen. 14, 200–204 (2007).

    Article  CAS  PubMed  Google Scholar 

  141. Fracheboud, J. et al. Interval cancers in the Dutch breast cancer screening programme. Br. J. Cancer 81, 912–917 (1999).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  142. Breast Cancer Surveillance Consortium. Evaluating screening performance in practice. NIH National Cancer Institute [online], (2004).

  143. Centers for Medicare & Medicaid Services. Decision memo for screening for lung cancer with low dose computed tomography (LDCT) (CAG-00439N). [online], (2015).

  144. Yourman, L. C., Lee, S. J., Schonberg, M. A., Widera, E. W. & Smith, A. K. Prognostic indices for older adults: a systematic review. JAMA 307, 182–192 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  145. Stacey, D. et al. Decision aids for people facing health treatment or screening decisions. Cochrane Database Syst. Rev. 1, CD001431 (2014).

    Google Scholar 

  146. The Canadian Task Force on Preventive Health Care. Recommendations on screening for breast cancer in average-risk women aged 40–74 years. CMAJ 183, 1991–2001 (2011).

  147. The Royal Australian College of General Practitioners. Guidelines for preventive activities in general practice, 8th edition. [online]

Download references

Acknowledgements

We wish to thank Michael Pignone, MD, of the University of North Carolina at Chapel Hill, USA, for his thoughtful editing of this manuscript. We also wish to thank Alexandra Barratt, PhD, of the University of Sydney, Australia, for her helpful discussions and communications regarding cervical-cancer screening. Lastly, we wish to thank Mamta Shah of the University of California, San Francisco, USA, for her assistance in creating the draft figures for our manuscript.

Author information

Authors and Affiliations

Authors

Contributions

All authors researched the data for article, contributed substantially to discussions of content and reviewed/edited the manuscript before submission. Y.S. and L.J.E. wrote the manuscript.

Corresponding author

Correspondence to Laura J. Esserman.

Ethics declarations

Competing interests

M.E. is named on four patents applications for prostate-cancer diagnostics. G.F.S. is Principal Investigator of an NCI-funded grant that aims to identify the range of reasonable options for cervical-cancer screening from a patient-centred and economic perspective (R011CA169093). Y.S., W.C.B., B.S.K., and L.J.E. declare no competing interests.

Related links

FURTHER INFORMATION

e-Prognosis

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shieh, Y., Eklund, M., Sawaya, G. et al. Population-based screening for cancer: hope and hype. Nat Rev Clin Oncol 13, 550–565 (2016). https://doi.org/10.1038/nrclinonc.2016.50

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrclinonc.2016.50

This article is cited by

Search

Quick links

Nature Briefing: Cancer

Sign up for the Nature Briefing: Cancer newsletter — what matters in cancer research, free to your inbox weekly.

Get what matters in cancer research, free to your inbox weekly. Sign up for Nature Briefing: Cancer