Clinical Guidelines19 May 2015

Screening for Cancer: Advice for High-Value Care From the American College of Physicians

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    Abstract

    Background

    Cancer screening is one approach to reducing cancer-related morbidity and mortality rates. Screening strategies vary in intensity. Higher-intensity strategies are not necessarily higher value. High-value strategies provide a degree of benefits that clearly justifies the harms and costs incurred; low-value screening provides limited or no benefits to justify the harms and costs. When cancer screening leads to benefits, an optimal intensity of screening maximizes value. Some aspects of screening practices, especially overuse and underuse, are low value.

    Methods

    Screening strategies for asymptomatic, average-risk adults for 5 common types of cancer were evaluated by reviewing clinical guidelines and evidence syntheses from the American College of Physicians (ACP), U.S. Preventive Services Task Force, American Academy of Family Physicians, American Cancer Society, American Congress of Obstetricians and Gynecologists, American Gastroenterological Association, and American Urological Association. “High value” was defined as the lowest screening intensity threshold at which organizations agree about screening recommendations for each type of cancer and “low value” as agreement about not recommending overly intensive screening strategies. This information is supplemented with additional findings from randomized, controlled trials; modeling studies; and studies of costs or resource use, including information found in the National Cancer Institute's Physician Data Query and UpToDate.

    Conclusion

    The ACP provides high-value care screening advice for 5 common types of cancer; the specifics are outlined in this article. The ACP strongly encourages clinicians to adopt a cancer screening strategy that focuses on reaching all eligible persons with these high-value screening options while reducing overly intensive, low-value screening.

    Cancer is a major health problem in the United States, causing 1 in 4 deaths (1). One approach to reducing cancer morbidity and mortality rates is screening. However, even full implementation of effective screening strategies would not eliminate cancer deaths.

    Screening strategies vary in what we call “intensity” (2). Higher-intensity strategies screen broader populations more frequently or with more sensitive screening tests. Screening strategies also vary in value. As defined by the American College of Physicians (ACP) (3–5), value is determined by an intervention's health benefits versus its harms and costs. High-value strategies return large health benefits for the harms and costs incurred; low-value strategies return disproportionately small benefits for the harms and costs. Although high-intensity strategies aim to maximize cancer detection, value is optimized by finding the level of intensity that best balances benefits with harms and costs (2).

    Regardless of value, cancer screening is popular among the U.S. public and is done more frequently than in other countries (6–8). Some aspects of our screening practices, especially overuse and underuse, are low value. A screening program is considered low value when persons in whom the benefits clearly outweigh the harms and costs are not being screened intensively enough (9, 10) or when persons are being screened overly intensively (11).

    Improving cancer screening value requires overcoming 3 main challenges: increasing access to high-value screening for populations without adequate access to care; increasing high-value screening in persons with adequate care access; and reducing use of low-value screening strategies in everyone, with or without adequate access. This article focuses on the latter 2 challenges. It is the second of 2 papers commissioned by the ACP to define and encourage high-value, cost-conscious cancer screening. We note agreement among various organizations on the lowest-intensity screening threshold recommended for “average-risk individuals” for each type of cancer (high value) and whether they recommend against or do not recommend for more intensive screening strategies (low value). We provide information on use of overly intensive, low-value screening and end with evidence suggesting future directions to reduce overly intensive screening that may enhance cancer screening value.

    Methods

    We focused on 5 common types of cancer: breast, cervical, colorectal, ovarian, and prostate. This article is intended to provide advice rather than to serve as a guideline. It is based on a narrative review of clinical guidelines and evidence syntheses from the American College of Physicians (ACP), U.S. Preventive Services Task Force, American Cancer Society, American Academy of Family Physicians, American Congress of Obstetricians and Gynecologists, American Urological Association, and American Gastroenterological Association. Because these organizations usually do not estimate costs in their recommendations, we searched the National Cancer Institute's Physician Data Query system, UpToDate, and modeling studies from the National Cancer Institute's Cancer Intervention and Surveillance Modeling Network for additional evidence from randomized, controlled trials (RCTs) or models of screening effectiveness, as well as national studies of the costs of various screening strategies for our target types of cancer. We searched MEDLINE for articles about the costs and resource use of cancer screening published within the past 5 years (1 January 2009 to 30 June 2014) in the following medical journals: Annals of Internal Medicine, The Journal of the American Medical Association (JAMA), JAMA Internal Medicine, Journal of General Internal Medicine, The New England Journal of Medicine, BMJ, The Lancet, Journal of the National Cancer Institute, Obstetrics & Gynecology, and CA: A Cancer Journal for Clinicians. We examined reference lists of articles to find further studies.

    For each type of cancer, we listed the least intensive screening strategies that all organizations recommend (defined as high-value care) and strategies that organizations either did not recommend or recommended against (defined as low-value care). The ACP used this information to develop high-value care advice statements. We used articles identified previously to suggest future directions that might enhance screening value by reducing overuse of overly intensive screening. Although the ACP High Value Care Task Force does not include evidence about costs in its advice statements, cost is still an important part of the “value framework” developed by the authors (2). We provide examples from national studies about overuse of nonrecommended strategies.

    We focus on screening average-risk, asymptomatic adults. We do not address surveillance in patients with previous abnormal screening results or high-risk populations. Our understanding of factors, beyond patient age or a history of cancer in multiple family members or in an immediate family member at an early age, that have both clinically important effects on cancer risk and health outcomes due to screening is limited. Value may differ for persons at higher or lower risk for cancer mortality. Value may also differ based on any individual patient (and physician) weighting of population estimates of benefits, harms, and costs.

    This article was reviewed and approved by the High Value Care Task Force, whose members are physicians trained in internal medicine and its subspecialties and experts in evidence synthesis. The Task Force developed the high-value care advice statements on the basis of a narrative review of the literature. At each conference call, all members declared all financial and nonfinancial interests. The target audience for this paper is all clinicians. The target patient population is average-risk, asymptomatic persons.

    Results
    Breast Cancer

    On the basis of RCTs and corresponding modeling studies, all groups recommend mammography screening, or discussions about screening, at least every 2 years for women aged 40 to 74 years (Table 1 and Appendix Table 1,) (9, 12–14). No group recommends regular systematic breast self-examination, magnetic resonance imaging (MRI), or tomosynthesis screening for average-risk women. Evidence is insufficient on the benefits of clinical breast examination beyond mammography alone (15). Reasons for not recommending more intensive strategies (such as annual screening, screening younger or older age groups, screening persons of any age with a life expectancy less than 10 years, and screening with more sensitive tests) include concerns that they would lead to few benefits but large increases in harms, such as false-positive screening test results and overdiagnosis and overtreatment of lesions that would never have progressed to cause clinical problems (16–20). Screening costs would also greatly increase (21).

    Table 1. High- and Low-Value Screening Strategies for 5 Types of Cancer

    Table 1.

    Appendix Table 1. Cancer Screening Recommendations of the ACP, USPSTF, AAFP, ACS, and Professional Societies

    Appendix Table 1.

    High-value care advice 1: Clinicians should discuss the benefits and harms of screening mammography with average-risk women aged 40 to 49 years and order biennial mammography screening if an informed woman requests it.

    High-value care advice 2: Clinicians should encourage biennial mammography screening in average-risk women aged 50 to 74 years.

    High-value care advice 3: Clinicians should not screen average-risk women younger than 40 years or aged 75 years or older for breast cancer or screen women of any age with a life expectancy less than 10 years.

    High-value care advice 4: Clinicians should not screen average-risk women of any age for breast cancer with MRI or tomosynthesis.

    Cervical Cancer

    On the basis of strong and consistent observational and modeling studies, all organizations recommend starting screening with cytology every 3 years at age 21 years, regardless of sexual history (Appendix Table 1 and Table 1) (9, 13, 22, 23). At age 30 years, women have the choice of continuing cytology screening every 3 years or cotesting with cytology plus human papillomavirus (HPV) testing every 5 years. For women with previously negative test results, screening can be safely stopped at age 65 years. The reasons for not screening women younger than 21 years or older than 65 years and for reducing screening frequency to every 3 to 5 years rather than every year include the concern that more intensive screening would lead to few benefits but many more harms, including increased psychological and physical complications from colposcopy follow-up of false-positive screening test results, overdiagnosis, overtreatment, and higher costs.

    High-value care advice 5: Clinicians should not screen average-risk women younger than 21 years for cervical cancer.

    High-value care advice 6: Clinicians should start screening average-risk women for cervical cancer at age 21 years once every 3 years with cytology (Papanicolaou [Pap] tests without HPV tests).

    High-value care advice 7: Clinicians should not screen average-risk women for cervical cancer with cytology more often than once every 3 years.

    High-value care advice 8: Clinicians may use a combination of Pap and HPV testing once every 5 years in average-risk women aged 30 years or older who prefer screening less often than every 3 years.

    High-value care advice 9: Clinicians should not perform HPV testing in average-risk women younger than 30 years.

    High-value care advice 10: Clinicians should stop screening average-risk women older than 65 years for cervical cancer who have had 3 consecutive negative cytology results or 2 consecutive negative cytology plus HPV test results within 10 years, with the most recent test done within 5 years.

    High-value care advice 11: Clinicians should not screen average-risk women of any age who have had a hysterectomy with removal of the cervix for cervical cancer.

    High-value care advice 12: Clinicians should not perform cervical cancer screening with a bimanual pelvic examination.

    Colorectal Cancer

    On the basis of results from RCTs of screening (fecal occult blood test [FOBT] and sigmoidoscopy) and consistent observational studies, all organizations recommend screening persons aged 50 to 75 years with 1 of 4 strategies: high-sensitivity FOBT or fecal immunochemical test (FIT) (every year); sigmoidoscopy (every 5 years); combined high-sensitivity FOBT or FIT (every 3 years) plus sigmoidoscopy (every 5 years); or optical colonoscopy (every 10 years) (Appendix Table 1 and Table 1) (9, 13, 24–27). The U.S. Food and Drug Administration approved a new DNA stool test, Cologuard (Exact Sciences), for which more comparative effectiveness data are needed. More intensive screening strategies, such as starting at a younger age, continuing to an older age, screening more frequently than recommended, or screening with tests not yet recommended, would be of lower value because benefits would increase only slightly while costs and harms would increase greatly, including complications due to more colonoscopies, overdiagnosis, and overtreatment (26, 28–30).

    High-value care advice 13: Clinicians should encourage colorectal cancer screening by 1 of 4 strategies: high-sensitivity FOBT or FIT (every year); sigmoidoscopy (every 5 years); combined high-sensitivity FOBT or FIT (every 3 years) plus sigmoidoscopy (every 5 years); or optical colonoscopy (every 10 years) in average-risk adults aged 50 to 75 years.

    High-value care advice 14: Clinicians should not screen for colorectal cancer more frequently than recommended in the 4 strategies mentioned previously.

    High-value care advice 15: Clinicians should not conduct interval screening with fecal testing or flexible sigmoidoscopy in adults having 10-year screening colonoscopy.

    High-value care advice 16: Clinicians should not screen for colorectal cancer in average-risk adults younger than 50 years or older than 75 years or those with an estimated life expectancy of less than 10 years.

    Ovarian Cancer

    Based on a large RCT of screening, all organizations recommend against pelvic examinations, cancer antigen 125 blood tests, and transvaginal ultrasonography for ovarian cancer screening (Appendix Table 1 and Table 1) (9, 13, 31–33). Screening would lead to no benefits and would increase harms and costs, including complications of invasive work-ups.

    High-value care advice 17: Clinicians should not screen average-risk women for ovarian cancer.

    Prostate Cancer

    On the basis of RCT findings, no organization recommends prostate-specific antigen (PSA) testing for prostate cancer screening without a discussion of benefits and harms and a patient's expressed, clear preference for screening (Appendix Table 1 and Table 1) (9, 13, 34–36). The primary target group is men aged 50 to 69 years. More intensive screening, including widespread testing in the absence of a request from a well-informed patient to be screened or among men older or younger than the target group, would lead to small incremental benefits, at most, with a larger increase in costs and harms, especially from prostate biopsy and overdiagnosis and overtreatment (37–39). The role of screening digital rectal examinations by trained clinicians, either alone or with PSA cotesting if the digital rectal examination result is abnormal, has not been well-studied. This strategy would likely reduce overdiagnosis and overtreatment compared with broad-based PSA screening and may decrease mortality rates compared with no prostate cancer screening (34).

    High-value care advice 18: Clinicians should have a 1-time discussion (more if the patient requests them) with average-risk men aged 50 to 69 years who inquire about PSA-based prostate cancer screening to inform them about the limited potential benefits and substantial harms of screening for prostate cancer using the PSA test.

    High-value care advice 19: Clinicians should not screen for prostate cancer using the PSA test in average-risk men aged 50 to 69 years who have not had an informed discussion and do not express a clear preference for screening.

    High-value care advice 20: Clinicians should not screen for prostate cancer using the PSA test in average-risk men younger than 50 years or older than 69 years or those with a life expectancy of less than 10 years.

    Future Directions: Enhancing Cancer Screening Value by Reducing Overly Intensive Screening

    An important step to improving cancer screening value is to increase implementation of underused strategies in which benefits clearly justify harms and costs. This is an important problem, especially in populations with inadequate access to care. We list 6 key principles that could enhance future cancer screening value by reducing overly intensive screening (Table 2). In Appendix Table 2, we provide the types of additional evidence needed before widespread implementation, as well as selected preliminary evidence that supports these principles. The results of the presented studies should stimulate consideration for future research and implementation of strategies to enhance screening value by reducing overly intensive screening. The identified studies are not based on a systematic search and are not definitive. Findings are primarily based on single studies or modeling or cost analyses requiring several assumptions. Other suggestive evidence comes from subgroup results from randomized trials. Further research confirming these findings is needed before widespread implementation, but they may hold promise for future, higher-value strategies that involve less-intensive screening. Few studies considered by guideline developers or in our additional searches examined harms and costs to the same degree that they examined benefits. Thus, few studies and corresponding guideline developers could directly assess the value of the screening strategy they were investigating.

    Table 2. Future Directions to Reduce Screening Intensity That May Further Enhance Cancer Screening Value

    Table 2.

    Appendix Table 2. Future Evidence Required Before Implementation of, and Selected Current Evidence Supporting, Reduced Screening Intensity That May Further Enhance Cancer Screening Value

    Appendix Table 2.
    How Common Is Overly Intensive, Low-Value Screening?

    Overly intensive, low-value screening is common. For example, 20% of women aged 30 to 39 years received a physician recommendation for mammography, and 23% to 35% in this age group had mammography (40). Most women having mammography receive it annually. One third of surveyed primary care physicians screen with ultrasonography and MRI, in addition to mammography, in women who are not at increased risk for breast cancer. Claims data demonstrate high use of screening MRI in women who are not at increased risk (41). Among women aged 80 years or older, cervical and breast cancer screening occurs in 38% and 50%, respectively (19). Cervical cancer screening is commonly done earlier and more frequently than recommended (42). Nearly 70% of women without a cervix received a Pap test for cervical cancer screening in 2002 (43). An estimated 1.2 million U.S. women have ovarian cancer screening (44). More than 40% of responding internists and nearly all gynecologists report performing annual pelvic examinations for ovarian or other gynecologic cancer screening (45).

    Inappropriate colorectal cancer screening is also common. Sixty percent of adults had colonoscopies more frequently than guidelines recommend, and screening often occurs in adults with life expectancies of 5 years or less (46–48). Among persons having an FOBT screening test, 8% had a negative result less than 1 year before (49). One third of men having PSA testing do not recall being told that the test was ordered (50). Most persons having PSA testing received annual cancer screening, and one half of men aged 75 to 79 years had recent screening. More than 50% of men and women older than 75 years report that their physicians continue to recommend screening (51).

    Discussion

    The ACP strongly encourages considering value in making health care decisions (4). Our growing appreciation of the problems of overly intensive, low-value care, including unjustifiable harms and costs, should lead us to consider value in many areas of health care. Cancer screening is no exception.

    We summarized cancer screening recommendations for 5 common types of cancer, finding much agreement about acceptable minimal screening strategies and not recommending overly intensive strategies. Guideline groups are increasingly considering value in terms of balancing benefits and harms in making cancer screening recommendations. This value consideration is associated with greater agreement on recommendations for screening for specific types of cancer. Although disagreement remains in some areas, such as annual (9) versus biennial (14) mammography screening for breast cancer, it is possible to develop a list of generally agreed-on, less intensive strategies that we define as high value. This consensus should be seen as a remarkable achievement.

    In addition to generally acceptable, high-value screening strategies, we found much agreement about recommending against or not recommending overly intensive, low-value screening. Recommendations have trended toward less-intensive screening and may foreshadow further discussion about screening intensity and value. We believe that this trend enhances screening value, chiefly by forgoing the small incremental benefits of more intensive screening as not being justified by the increase in harms. Although these organizations do not make recommendations based on financial costs, less-intensive, high-value screening is less expensive than overly intensive screening. We also found evidence that overly intensive and thus low-value care is common. In addition, underutilization of high-value care exists, especially among persons with limited health care access. Thus, clinicians can markedly improve cancer screening value by adhering to the widely agreed-on, high- and low-value strategies recommended by the High Value Care Task Force.

    Further enhancing value may be possible through implementation of less rather than more intensive screening. We provided preliminary evidence and a value framework suggesting additional strategies that could enhance value through less intensive screening for clinicians, researchers, policymakers, and patients to consider. However, implementation will require additional research consistently demonstrating that less-intensive screening leads to little loss in benefits and larger reductions in harms and costs. Guideline groups and researchers need to better clarify which screening strategies represent high or low value. Guideline developers can help clinicians determine the value of screening strategies by searching for evidence about health benefits, harms, and costs and then carefully analyzing tradeoffs. For some organizations, this would be a departure because they may not adequately consider evidence about harms and often do not assess costs. To improve the value of screening (and health care in general), harms and costs should be considered equally with benefits to explicitly assess value. Clinicians should pay special attention to transparent recommendations from organizations that are rigorous in making these determinations.

    Researchers play an essential role in determining and enhancing the value of screening strategies. For persons with repeated negative test results, research should consider the additional value of continued screening. Research should also consider how much benefit would be lost and how much harms and costs would be reduced by screening less frequently; using a higher test threshold to define abnormality; or screening a smaller, higher-risk population. It would be difficult to consider these questions under a “maximum cancer detection” framework, but they become priority questions under a value framework (2). Research must focus on the consequences of the full screening cascade, including a better understanding of what constitutes “overdiagnosed cancer” and how to reduce overdiagnosis and overtreatment (52). It should also focus on approaches clinicians can use to communicate the benefits, harms, and costs of screening to their patients and society, including ways of incorporating the concept of value.

    Considering screening through the lens of value could change discussions between clinicians and patients. Rather than assuming that all screening is high-value, clinicians might start a conversation with the understanding that it always involves tradeoffs between benefits versus harms and costs and that some patients may reasonably decide that they would prefer less intensive screening. Further, considering the patient's situation and own weighting of benefits and harms may lead him or her to conclude that cancer screening is not the highest priority and that there may be other more pressing issues to discuss.

    In conclusion, we advise clinicians to consider value when discussing cancer screening with their patients. Implementation of high-value strategies and avoidance of the overly intensive, low-value strategies that we outlined as widely agreed-on would increase cancer screening value. In addition, an emphasis on enhancing value by decreasing harms and costs while preserving most benefits may resonate with many patients. Low-value screening can result from strategies that are either too low or too high in intensity. We have focused on the problem of overly intensive strategies that lead to low value. Reducing overly intensive, low-value screening would not only reduce screening harms and costs but also release time and resources to increase intensity among underserved groups, thus further improving value.

    References

    • 1. Siegel RLMiller KDJemal ACancer statistics, 2015. CA Cancer J Clin2015;65:5-29. [PMID: 25559415] doi:10.3322/caac.21254 CrossrefMedlineGoogle Scholar
    • 2. Harris RPWilt TJQaseem AHigh Value Care Task Force of the American College of PhysiciansA value framework for cancer screening: advice for high-value care from the American College of Physicians. Ann Intern Med2015;162:712-7. doi:10.7326/M14-5304 LinkGoogle Scholar
    • 3. Baker DWQaseem AReynolds PPGardner LASchneider ECAmerican College of Physicians Performance Measurement CommitteeDesign and use of performance measures to decrease low-value services and achieve cost-conscious care. Ann Intern Med2013;158:55-9. [PMID: 23108285] LinkGoogle Scholar
    • 4. Owens DKQaseem AChou RShekelle PClinical Guidelines Committee of the American College of PhysiciansHigh-value, cost-conscious health care: concepts for clinicians to evaluate the benefits, harms, and costs of medical interventions. Ann Intern Med2011;154:174-80. [PMID: 21282697] doi:10.7326/0003-4819-154-3-201102010-00007 LinkGoogle Scholar
    • 5. Qaseem AAlguire PDallas PFeinberg LEFitzgerald FTHorwitch Cet alAppropriate use of screening and diagnostic tests to foster high-value, cost-conscious care. Ann Intern Med2012;156:147-9. [PMID: 22250146] doi:10.7326/0003-4819-156-2-201201170-00011 LinkGoogle Scholar
    • 6. Bellizzi KMBreslau ESBurness AWaldron WPrevalence of cancer screening in older, racially diverse adults: still screening after all these years. Arch Intern Med2011;171:2031-7. [PMID: 22158573] doi:10.1001/archinternmed.2011.570 CrossrefMedlineGoogle Scholar
    • 7. Howard DHRichardson LCThorpe KECancer screening and age in the United States and Europe. Health Aff (Millwood)2009;28:1838-47. [PMID: 19887425] doi:10.1377/hlthaff.28.6.1838 CrossrefMedlineGoogle Scholar
    • 8. Schwartz LMWoloshin SFowler FJWelch HGEnthusiasm for cancer screening in the United States. JAMA2004;291:71-8. [PMID: 14709578] CrossrefMedlineGoogle Scholar
    • 9. Smith RAManassaram-Baptiste DBrooks DDoroshenk MFedewa SSaslow Det alCancer screening in the United States, 2015: a review of current American Cancer Society guidelines and current issues in cancer screening. CA Cancer J Clin2015;65:30-54. [PMID: 25581023] doi:10.3322/caac.21261 CrossrefMedlineGoogle Scholar
    • 10. Curry SJByers THewitt MedsFulfilling the Potential of Cancer Prevention and Early Detection. Washington, DC: National Academies Pr; 2003. Google Scholar
    • 11. Baker DWQaseem AReynolds PPGardner LASchneider ECAmerican College of Physicians Performance Measurement CommitteeDesign and use of performance measures to decrease low-value services and achieve cost-conscious care. Ann Intern Med2013;158:55-9. [PMID: 23108285] LinkGoogle Scholar
    • 12. Qaseem ASnow VSherif KAronson MWeiss KBOwens DKClinical Efficacy Assessment Subcommittee of the American College of PhysiciansScreening mammography for women 40 to 49 years of age: a clinical practice guideline from the American College of Physicians. Ann Intern Med2007;146:511-5. [PMID: 17404353] LinkGoogle Scholar
    • 13. American Academy of Family Physicians. Summary of Recommendations for Clinical Preventive Services. 2015. Accessed at www.aafp.org/dam/AAFP/documents/patient_care/clinical_recommendations/cps-recommendations.pdf on 3 April 2015. Google Scholar
    • 14. U.S. Preventive Services Task ForceScreening for breast cancer: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med2009;151:716-26. [PMID: 19920272] doi:10.7326/0003-4819-151-10-200911170-00008 LinkGoogle Scholar
    • 15. National Cancer Institute. Breast Cancer Screening (PDQ). Bethesda, MD: National Cancer Institute; 2014. Accessed at www.cancer.gov/cancertopics/pdq/screening/breast/healthprofessional on 7 October 2014. Google Scholar
    • 16. Welch HGPassow HJQuantifying the benefits and harms of screening mammography. JAMA Intern Med2014;174:448-54. [PMID: 24380095] doi:10.1001/jamainternmed.2013.13635 CrossrefMedlineGoogle Scholar
    • 17. Pace LEKeating NLA systematic assessment of benefits and risks to guide breast cancer screening decisions. JAMA2014;311:1327-35. [PMID: 24691608] doi:10.1001/jama.2014.1398 CrossrefMedlineGoogle Scholar
    • 18. Gross CPLong JBRoss JSAbu-Khalaf MMWang RKillelea BKet alThe cost of breast cancer screening in the Medicare population. JAMA Intern Med2013;173:220-6. [PMID: 23303200] doi:10.1001/jamainternmed.2013.1397 CrossrefMedlineGoogle Scholar
    • 19. Walter LCSchonberg MAScreening mammography in older women: a review. JAMA2014;311:1336-47. [PMID: 24691609] doi:10.1001/jama.2014.2834 CrossrefMedlineGoogle Scholar
    • 20. Lee SJBoscardin WJStijacic-Cenzer IConell-Price JO'Brien SWalter LCTime lag to benefit after screening for breast and colorectal cancer: meta-analysis of survival data from the United States, Sweden, United Kingdom, and Denmark. BMJ2013;346:e8441. [PMID: 23299842] doi:10.1136/bmj.e8441 CrossrefMedlineGoogle Scholar
    • 21. O'Donoghue CEklund MOzanne EMEsserman LJAggregate cost of mammography screening in the United States: comparison of current practice and advocated guidelines. Ann Intern Med2014;160:145. [PMID: 24658691] doi:10.7326/M13-1217 LinkGoogle Scholar
    • 22. Moyer VAU. S. Preventive Services Task ForceScreening for cervical cancer: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med2012;156:880-91. [PMID: 22711081] doi:10.7326/0003-4819-156-12-201206190-00424 LinkGoogle Scholar
    • 23. Sawaya GFKulasingam SDenberg TQaseem AClinical Guidelines Committee of the American College of PhysiciansCervical cancer screening in average-risk patients: best practice advice from the Clinical Guidelines Committee of the American College of Physicians. Ann Intern Med2015 [Epub ahead of print 30 April 2015]. doi:10.7326/M14-2426 LinkGoogle Scholar
    • 24. U.S. Preventive Services Task ForceScreening for colorectal cancer: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med2008;149:627-37. [PMID: 18838716] LinkGoogle Scholar
    • 25. Levin BLieberman DAMcFarland BAndrews KSBrooks DBond Jet alAmerican Cancer Society Colorectal Cancer Advisory GroupScreening and surveillance for the early detection of colorectal cancer and adenomatous polyps, 2008: a joint guideline from the American Cancer Society, the U.S. Multi-Society Task Force on Colorectal Cancer, and the American College of Radiology. Gastroenterology2008;134:1570-95. [PMID: 18384785] doi:10.1053/j.gastro.2008.02.002 CrossrefMedlineGoogle Scholar
    • 26. Qaseem ADenberg TDHopkins RHHumphrey LLLevine JSweet DEet alClinical Guidelines Committee of the American College of PhysiciansScreening for colorectal cancer: a guidance statement from the American College of Physicians. Ann Intern Med2012;156:378-86. [PMID: 22393133] doi:10.7326/0003-4819-156-5-201203060-00010 LinkGoogle Scholar
    • 27. Winawer SJZauber AGFletcher RHStillman JSO'Brien MJLevin Bet alGuidelines for colonoscopy surveillance after polypectomy: a consensus update by the U.S. Multi-Society Task Force on Colorectal Cancer and the American Cancer Society. CA Cancer J Clin2006;56:143-59; quiz 184-5. [PMID: 16737947] CrossrefMedlineGoogle Scholar
    • 28. Lansdorp-Vogelaar IKnudsen ABBrenner HCost-effectiveness of colorectal cancer screening. Epidemiol Rev2011;33:88-100. [PMID: 21633092] doi:10.1093/epirev/mxr004 CrossrefMedlineGoogle Scholar
    • 29. Warren JLKlabunde CNMariotto ABMeekins ATopor MBrown MLet alAdverse events after outpatient colonoscopy in the Medicare population. Ann Intern Med2009;150:849-57. [PMID: 19528563] LinkGoogle Scholar
    • 30. Knudsen ABLansdorp-Vogelaar IRutter CMSavarino JEvan Ballegooijen MKuntz KMet alCost-effectiveness of computed tomographic colonography screening for colorectal cancer in the Medicare population. J Natl Cancer Inst2010;102:1238-52. [PMID: 20664028] doi:10.1093/jnci/djq242 CrossrefMedlineGoogle Scholar
    • 31. Buys SSPartridge EBlack AJohnson CCLamerato LIsaacs Cet alPLCO Project TeamEffect of screening on ovarian cancer mortality: the Prostate, Lung, Colorectal and Ovarian (PLCO) Cancer Screening Randomized Controlled Trial. JAMA2011;305:2295-303. [PMID: 21642681] doi:10.1001/jama.2011.766 CrossrefMedlineGoogle Scholar
    • 32. Qaseem AHumphrey LLHarris RStarkey MDenberg TDClinical Guidelines Committee of the American College of PhysiciansScreening pelvic examination in adult women: a clinical practice guideline from the American College of Physicians. Ann Intern Med2014;161:67-72. [PMID: 24979451] doi:10.7326/M14-0701 LinkGoogle Scholar
    • 33. Moyer VAU. S. Preventive Services Task ForceScreening for ovarian cancer: U.S. Preventive Services Task Force reaffirmation recommendation statement. Ann Intern Med2012;157:900-4. [PMID: 22964825] doi:10.7326/0003-4819-157-11-201212040-00539 LinkGoogle Scholar
    • 34. Moyer VAU.S. Preventive Services Task ForceScreening for prostate cancer: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med2012;157:120-34. [PMID: 22801674] doi:10.7326/0003-4819-157-2-201207170-00459 LinkGoogle Scholar
    • 35. Qaseem ABarry MJDenberg TDOwens DKShekelle PClinical Guidelines Committee of the American College of PhysiciansScreening for prostate cancer: a guidance statement from the Clinical Guidelines Committee of the American College of Physicians. Ann Intern Med2013;158:761-9. [PMID: 23567643] doi:10.7326/0003-4819-158-10-201305210-00633 LinkGoogle Scholar
    • 36. Carter HB, Albertsen PC, Barry MJ, Etzioni R, Freedland SJ, Greene KL, et al. Early Detection of Prostate Cancer: AUA Guideline. Accessed at www.auanet.org/education/guidelines/prostate-cancer-detection.cfm on 16 March 2015. Google Scholar
    • 37. Ma XWang RLong JBRoss JSSoulos PRYu JBet alThe cost implications of prostate cancer screening in the Medicare population. Cancer2014;120:96-102. [PMID: 24122801] doi:10.1002/cncr.28373 CrossrefMedlineGoogle Scholar
    • 38. Pataky RGulati REtzioni RBlack PChi KNColdman AJet alIs prostate cancer screening cost-effective? A microsimulation model of prostate-specific antigen-based screening for British Columbia, Canada. Int J Cancer2014;135:939-47. [PMID: 24443367] doi:10.1002/ijc.28732 CrossrefMedlineGoogle Scholar
    • 39. Shteynshlyuger AAndriole GLCost-effectiveness of prostate specific antigen screening in the United States: extrapolating from the European study of screening for prostate cancer. J Urol2011;185:828-32. [PMID: 21239021] doi:10.1016/j.juro.2010.10.079 CrossrefMedlineGoogle Scholar
    • 40. Kapp JMYankaskas BCLeFevre MLAre mammography recommendations in women younger than 40 related to increased risk? Breast Cancer Res Treat2010;119:485-90. [PMID: 19148745] doi:10.1007/s10549-008-0305-x CrossrefMedlineGoogle Scholar
    • 41. Stout NKNekhlyudov LLi LMalin ESRoss-Degnan DBuist DSet alRapid increase in breast magnetic resonance imaging use: trends from 2000 to 2011. JAMA Intern Med2014;174:114-21. [PMID: 24247482] doi:10.1001/jamainternmed.2013.11958 CrossrefMedlineGoogle Scholar
    • 42. Berkowitz ZSaraiya MSawaya GFCervical cancer screening intervals, 2006 to 2009: moving beyond annual testing [Letter]. JAMA Intern Med2013;173:922-4. [PMID: 23568334] doi:10.1001/jamainternmed.2013.368 CrossrefMedlineGoogle Scholar
    • 43. Sirovich BEWelch HGCervical cancer screening among women without a cervix. JAMA2004;291:2990-3. [PMID: 15213211] CrossrefMedlineGoogle Scholar
    • 44. Baldwin LMTrivers KFMatthews BAndrilla CHMiller JWBerry DLet alVignette-based study of ovarian cancer screening: do U.S. physicians report adhering to evidence-based recommendations? Ann Intern Med2012;156:182-94. [PMID: 22312138] doi:10.7326/0003-4819-156-3-201202070-00006 LinkGoogle Scholar
    • 45. Stormo ARHawkins NACooper CPSaraiya MThe pelvic examination as a screening tool: practices of U.S. physicians [Letter]. Arch Intern Med2011;171:2053-4. [PMID: 22158576] doi:10.1001/archinternmed.2011.575 CrossrefMedlineGoogle Scholar
    • 46. Walter LCLindquist KNugent SSchult TLee SJCasadei MAet alImpact of age and comorbidity on colorectal cancer screening among older veterans. Ann Intern Med2009;150:465-73. [PMID: 19349631] LinkGoogle Scholar
    • 47. Korenstein DFalk RHowell EABishop TKeyhani SOveruse of health care services in the United States: an understudied problem. Arch Intern Med2012;172:171-8. [PMID: 22271125] doi:10.1001/archinternmed.2011.772 CrossrefMedlineGoogle Scholar
    • 48. Sheffield KMHan YKuo YFRiall TSGoodwin JSPotentially inappropriate screening colonoscopy in Medicare patients: variation by physician and geographic region. JAMA Intern Med2013;173:542-50. [PMID: 23478992] doi:10.1001/jamainternmed.2013.2912 CrossrefMedlineGoogle Scholar
    • 49. Partin MRPowell AABangerter AHalek KBurgess JFFisher DAet alLevels and variation in overuse of fecal occult blood testing in the Veterans Health Administration. J Gen Intern Med2012;27:1618-25. [PMID: 22810358] doi:10.1007/s11606-012-2163-9 CrossrefMedlineGoogle Scholar
    • 50. Walter LCBertenthal DLindquist KKonety BRPSA screening among elderly men with limited life expectancies. JAMA2006;296:2336-42. [PMID: 17105796] CrossrefMedlineGoogle Scholar
    • 51. Schwartz LMWoloshin SWelch HGNot so silver lining. Arch Intern Med2011;171:489-90. [PMID: 21444839] doi:10.1001/archinternmed.2011.73 CrossrefMedlineGoogle Scholar
    • 52. Etzioni RGulati RMallinger LMandelblatt JInfluence of study features and methods on overdiagnosis estimates in breast and prostate cancer screening. Ann Intern Med2013;158:831-8. [PMID: 23732716] doi:10.7326/0003-4819-158-11-201306040-00008 LinkGoogle Scholar
    • 53. de Kok IMvan Rosmalen JDillner JArbyn MSasieni PIftner Tet alPrimary screening for human papillomavirus compared with cytology screening for cervical cancer in European settings: cost effectiveness analysis based on a Dutch microsimulation model. BMJ2012;344:e670. [PMID: 22391612] doi:10.1136/bmj.e670 CrossrefMedlineGoogle Scholar
    • 54. Zauber AGLansdorp-Vogelaar IKnudsen ABWilschut Jvan Ballegooijen MKuntz KMEvaluating test strategies for colorectal cancer screening: a decision analysis for the U.S. Preventive Services Task Force. Ann Intern Med2008;149:659-69. [PMID: 18838717] LinkGoogle Scholar
    • 55. Atkin WSEdwards RKralj-Hans IWooldrage KHart ARNorthover JMet alUK Flexible Sigmoidoscopy Trial InvestigatorsOnce-only flexible sigmoidoscopy screening in prevention of colorectal cancer: a multicentre randomised controlled trial. Lancet2010;375:1624-33. [PMID: 20430429] doi:10.1016/S0140-6736(10)60551-X CrossrefMedlineGoogle Scholar
    • 56. Segnan NArmaroli PBonelli LRisio MSciallero SZappa Met alSCORE Working GroupOnce-only sigmoidoscopy in colorectal cancer screening: follow-up findings of the Italian Randomized Controlled Trial—SCORE. J Natl Cancer Inst2011;103:1310-22. [PMID: 21852264] doi:10.1093/jnci/djr284 CrossrefMedlineGoogle Scholar
    • 57. Holme ØLøberg MKalager MBretthauer MHernán MAAas Eet alEffect of flexible sigmoidoscopy screening on colorectal cancer incidence and mortality: a randomized clinical trial. JAMA2014;312:606-15. [PMID: 25117129] doi:10.1001/jama.2014.8266 CrossrefMedlineGoogle Scholar
    • 58. Schoen REPinsky PFWeissfeld JLYokochi LAChurch TLaiyemo AOet alPLCO Project TeamColorectal cancer incidence and mortality with screening flexible sigmoidoscopy. N Engl J Med2012;366:2345-57. [PMID: 22612596] doi:10.1056/NEJMoa1114635 CrossrefMedlineGoogle Scholar
    • 59. Kulasingam SLHavrilesky LGhebre RMyers ERScreening for cervical cancer: a decision analysis for the U.S. Preventive Services Task Force. AHRQ Publication No. 11-05157-EF-1. Rockville, MD: Agency for Healthcare Research and Quality; 2011. Google Scholar
    • 60. Imperiale TFGlowinski EALin-Cooper CLarkin GNRogge JDRansohoff DFFive-year risk of colorectal neoplasia after negative screening colonoscopy. N Engl J Med2008;359:1218-24. [PMID: 18799558] doi:10.1056/NEJMoa0803597 CrossrefMedlineGoogle Scholar
    • 61. Carlsson SAssel MSjoberg DUlmert DHugosson JLilja Het alInfluence of blood prostate specific antigen levels at age 60 on benefits and harms of prostate cancer screening: population based cohort study. BMJ2014;348:g2296. [PMID: 24682399] doi:10.1136/bmj.g2296 CrossrefMedlineGoogle Scholar
    • 62. Cho HKlabunde CNYabroff KRWang ZMeekins ALansdorp-Vogelaar Iet alComorbidity-adjusted life expectancy: a new tool to inform recommendations for optimal screening strategies. Ann Intern Med2013;159:667-76. [PMID: 24247672] doi:10.7326/0003-4819-159-10-201311190-00005 LinkGoogle Scholar
    • 63. Welch HGBlack WCOverdiagnosis in cancer. J Natl Cancer Inst2010;102:605-13. [PMID: 20413742] doi:10.1093/jnci/djq099 CrossrefMedlineGoogle Scholar
    • 64. Miller ABWall CBaines CJSun PTo TNarod SATwenty five year follow-up for breast cancer incidence and mortality of the Canadian National Breast Screening Study: randomised screening trial. BMJ2014;348:g366. [PMID: 24519768] doi:10.1136/bmj.g366 CrossrefMedlineGoogle Scholar
    • 65. Nelson HDTyne KNaik ABougatsos CChan BKHumphrey LU.S. Preventive Services Task ForceScreening for breast cancer: an update for the U.S. Preventive Services Task Force. Ann Intern Med2009;151:727-37. [PMID: 19920273] doi:10.7326/0003-4819-151-10-200911170-00009 LinkGoogle Scholar
    • 66. Goldhaber-Fiebert JDStout NKSalomon JAKuntz KMGoldie SJCost-effectiveness of cervical cancer screening with human papillomavirus DNA testing and HPV-16,18 vaccination. J Natl Cancer Inst2008;100:308-20. [PMID: 18314477] doi:10.1093/jnci/djn019 CrossrefMedlineGoogle Scholar
    • 67. Shaukat AMongin SJGeisser MSLederle FABond JHMandel JSet alLong-term mortality after screening for colorectal cancer. N Engl J Med2013;369:1106-14. [PMID: 24047060] doi:10.1056/NEJMoa1300720 CrossrefMedlineGoogle Scholar
    • 68. Stout NKLee SJSchechter CBKerlikowske KAlagoz OBerry Det alBenefits, harms, and costs for breast cancer screening after U.S. implementation of digital mammography. J Natl Cancer Inst2014;106:dju092. [PMID: 24872543] doi:10.1093/jnci/dju092 CrossrefMedlineGoogle Scholar
    • 69. Fenton JJLee CIXing GBaldwin LMElmore JGComputer-aided detection in mammography: downstream effect on diagnostic testing, ductal carcinoma in situ treatment, and costs. JAMA Intern Med2014;174:2032-4. [PMID: 25347134] doi:10.1001/jamainternmed.2014.5410 CrossrefMedlineGoogle Scholar
    • 70. Sprague BLStout NKSchechter Cvan Ravesteyn NTCevik MAlagoz Oet alBenefits, harms, and cost-effectiveness of supplemental ultrasonography screening for women with dense breasts. Ann Intern Med2015;162:157-66. [PMID: 25486550] doi:10.7326/M14-0692 LinkGoogle Scholar
    • 71. Andersson SOAndrén OLyth JStark JRHenriksson MAdami HOet alManaging localized prostate cancer by radical prostatectomy or watchful waiting: Cost analysis of a randomized trial (SPCG-4). Scand J Urol Nephrol2011;45::77-83. [PMID: 21265595] doi:10.3109/00365599.2010.545075 CrossrefMedlineGoogle Scholar
    • 72. Wilt TJBrawer MKJones KMBarry MJAronson WJFox Set alProstate Cancer Intervention versus Observation Trial (PIVOT) Study GroupRadical prostatectomy versus observation for localized prostate cancer. N Engl J Med2012;367:203-13. [PMID: 22808955] doi:10.1056/NEJMoa1113162 CrossrefMedlineGoogle Scholar
    • 73. Gupta SHalm EARockey DCHammons MKoch MCarter Eet alComparative effectiveness of fecal immunochemical test outreach, colonoscopy outreach, and usual care for boosting colorectal cancer screening among the underserved: a randomized clinical trial. JAMA Intern Med2013;173:1725-32. [PMID: 23921906] MedlineGoogle Scholar
    • 74. Welch HGSchwartz LMWoloshin SProstate-specific antigen levels in the United States: implications of various definitions for abnormal. J Natl Cancer Inst2005;97::132-7. [PMID: 16077071] CrossrefMedlineGoogle Scholar

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