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J Gen Intern Med. Aug 2007; 22(8): 1195–1205.
Published online May 30, 2007. doi:  10.1007/s11606-007-0231-3
PMCID: PMC2305744
Improving Colorectal Cancer Screening in Primary Care Practice: Innovative Strategies and Future Directions
Carrie N. Klabunde, Ph.D.,corresponding author1 David Lanier, M.D.,2 Erica S. Breslau, Ph.D.,3 Jane G. Zapka, Sc.D.,4 Robert H. Fletcher, M.D., M.Sc.,5 David F. Ransohoff, M.D.,6 and Sidney J. Winawer, M.D.7
1Health Services and Economics Branch, Applied Research Program, Division of Cancer Control and Population Sciences, National Cancer Institute, EPN 4005, 6130 Executive Boulevard, Bethesda, MD 20892-7344 USA
2Center for Primary Care, Prevention, and Clinical Partnerships, Agency for Healthcare Research and Quality, Rockville, MD USA
3Applied Cancer Screening Research Branch, Behavioral Research Program, Division of Cancer Control and Population Sciences, National Cancer Institute, Bethesda, MD USA
4Biostatistics, Bioinformatics and Epidemiology, Medical University of South Carolina, Charleston, SC USA
5Department of Ambulatory Care and Prevention, Harvard Medical School, Boston, MA USA
6School of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, NC USA
7Department of Medicine, Memorial Sloan-Kettering Cancer Center, New York, NY USA
Carrie N. Klabunde, Phone: +1-301-4023362, Fax: +1-301-4353710, klabundc/at/mail.nih.gov.
corresponding authorCorresponding author.
Received November 22, 2006; Revised April 2, 2007; Accepted April 6, 2007.
Colorectal cancer (CRC) screening has been supported by strong research evidence and recommended in clinical practice guidelines for more than a decade. Yet screening rates in the United States remain low, especially relative to other preventable diseases such as breast and cervical cancer. To understand the reasons, the National Cancer Institute and Agency for Healthcare Research and Quality sponsored a review of CRC screening implementation in primary care and a program of research funded by these organizations. The evidence base for improving CRC screening supports the value of a New Model of Primary Care Delivery: 1. a team approach, in which responsibility for screening tasks is shared among other members of the practice, would help address physicians’ lack of time for preventive care; 2. information systems can identify eligible patients and remind them when screening is due; 3. involving patients in decisions about their own care may enhance screening participation; 4. monitoring practice performance, supported by information systems, can help target patients at increased risk because of family history or social disadvantage; 5. reimbursement for services outside the traditional provider—patient encounter, such as telephone and e-mail contacts, may foster enhanced screening delivery; 6. training opportunities in communication, cultural competence, and use of information technologies would improve provider competence in core elements of screening programs. Improvement in CRC screening rates largely depends on the efforts of primary care practices to implement effective systems and procedures for screening delivery. Active engagement and support of practices are essential for the enormous potential of CRC screening to be realized.
KEY WORDS: colorectal cancer, screening, primary care, prevention
Evidence from clinical studies1 and guidelines from national expert groups24 support the use of several modalities to screen average-risk adults aged 50 years and older for colorectal cancer (CRC). The decentralized nature of health care delivery in the United States necessitates that primary care providers play a central role in implementing national guidelines by recommending, performing, and/or referring patients for CRC screening. Yet despite evidence and guidelines, CRC screening rates in the United States are considerably lower than screening rates for other types of cancer (Fig. 1). Although some office-based interventions to increase primary care providers’ use of CRC screening tests have been evaluated and shown to be efficacious,511 there is little evidence to suggest that they have been widely adopted into routine practice.12 Further, many primary care providers are already overburdened with the delivery of a broad range of medical care to their patients.13,14
Figure 1.
Figure 1.
Recent use of cancer screening tests from the 1987, 1992, 2000, and 2003 National Health Interview Surveys. Percentages are standardized to the 2000 projected U.S. population by 5-year age groups. Recent Pap smear is measured within the last 3 years for (more ...)
Practice pressures, widespread levels of dissatisfaction, and concern about the future have prompted 2 professional organizations, the Society of General Internal Medicine and the American Academy of Family Physicians, to delineate specific strategies for transforming primary care. These reports15,16 have particular relevance for CRC screening as the disciplines represented—general internal medicine and family medicine—are the most actively engaged in delivering preventive services to adults. The reports show what primary care practice might look like in the near future, and embrace 6 major elements of a new model of practice which, if implemented, would serve as the groundwork for improving the overall quality of primary care in the U.S. At the same time, the elements of this model describe an infrastructure that could facilitate the introduction into routine primary care of evidence-based strategies aimed at improving CRC screening rates.
Recognizing the critical need for more research to improve the uptake and delivery, and evaluate the short-term outcomes of CRC screening in primary care practice, the National Cancer Institute (NCI) and Agency for Healthcare Research and Quality (AHRQ) issued in December 2001 a program announcement (PAR-02-042/PAR 04-036, Colorectal Cancer Screening in Primary Care Practice) under which many innovative studies have been funded (see Appendix A). In April 2005, NCI and AHRQ convened a conference in Rockville, Maryland entitled “Improving Colorectal Cancer Screening Delivery, Utilization, and Outcomes: the State of the Science” that included several of the program’s grantees (see Appendix B for a listing of participants). This meeting provided a forum for describing and discussing innovative approaches to implementing CRC screening in primary care practice, challenges to widespread adoption of CRC screening, progress toward evaluating CRC screening at the population level, and research gaps. In this report, we use the framework of the New Model of Primary Care delivery15,16 to highlight evidence about interventions that could be implemented in primary care settings to increase CRC screening rates, describe current research supported by NCI and AHRQ to improve CRC screening in primary care practice, and note areas where more research is needed.
Through the NCI/AHRQ research program, it is likely that several evidence-based interventions for enhancing CRC screening uptake and delivery in the U.S. will be identified. However, this work—while important and necessary—will ultimately have value only if effective strategies are actually put to use in practice. An assumption of the NCI/AHRQ meeting was that evidence-based CRC screening strategies are more likely to be implemented and sustained when they are applied in the context of general efforts to provide high-quality care. Moreover, almost all of the intervention strategies discussed at the meeting could conceivably support practice improvements for other screening services in addition to CRC. Implementation of the strategies, however, requires a practice’s leadership to be prepared, proactive, and committed to providing high-quality care across the continuum of the practice.17 Many practices may need to make significant changes to their current approaches to care delivery to achieve this.
Assuring that such change occurs may be challenging. More than a decade of research has documented the difficulties physicians encounter in trying to alter established routines of care.1820 The knowledge, attitudes, or beliefs of the individual physician were initially thought to be barriers to change, and several studies of methods to improve care delivery have targeted these characteristics. Interventions that focus on the individual physician, however, have shown limited effectiveness in improving outcomes.21,22 More recent research has cast doubt on the consistency and strength of a relationship between physicians’ attitudes and preventive care delivery. It has been shown, for example, that, whereas most primary care physicians rate the delivery of preventive services as important or very important, in actuality, visit- and practice-specific factors largely determine whether these services are provided.23 Thus, the proposed strategies for improving CRC screening discussed at the NCI/AHRQ meeting primarily target systems of care rather than clinicians’ knowledge or attitudes alone.
Clinicians may be more receptive today to changing the way they practice than at any time in the recent past. Numerous observers have concluded that the pressures and frustrations characterizing today’s health care environment are providing an impetus for innovation, especially among primary care providers.24 As corporate interests and a business ethic have come to dominate U.S. health care, most primary care providers are struggling with increasing administrative burdens, lower reimbursement, and demands for brief visits.25,26 Their willingness to adopt new systems and approaches for improving care delivery may be reinforced by new requirements for measuring and reporting performance and quality. For example, CRC screening has recently been incorporated into several measure sets, including the Health Plan Employer Data Information Set (HEDIS) sponsored by the National Committee for Quality Assurance (http://www.ncqa.org/Programs/HEDIS/index.htm), and the National Quality Forum’s recommended “starter set” of clinical performance measures for ambulatory practices (http://www.qualityforum.org/txAmbCare-Summary-SC-TAP.pdf). Such measure sets may be a strong motivator for primary care practices to improve their CRC screening rates.
The studies funded by NCI and AHRQ address many of the elements of the New Model of Primary Care (Appendix A). A particularly unique and promising feature of this research portfolio is that most of the studies are being undertaken in community-based practices, several within primary care practice-based research networks (http://www.ahrq.gov/research/pbrnfact.htm), and nearly all in multiple clinic or office settings. This portfolio, however, represents a subset of published and in-progress research on CRC screening in primary care. Below, we broaden our consideration of innovative strategies for improving CRC screening in primary care practice by describing the elements of the New Model of Primary Care, highlighting for each the evidence base and research gaps related to CRC screening.
  • Team approach to care delivery.
    What is known. Whereas the physician has traditionally been considered the central figure of most primary care practices, the New Model acknowledges that health care of the future will no longer be delivered by a single individual. Instead, a multidisciplinary team will be used that may include—in addition to the physician—nurses, physician assistants, nurse practitioners, clerical personnel, and other health professionals such as health educators and behavioral scientists.
    A team approach can alter the way CRC screening is delivered by directly addressing the physician’s lack of time for preventive care. The shifting of certain responsibilities currently assumed to be the physician’s (e.g., determining screening eligibility; educating patients about CRC) to other members of the team will become increasingly important as the population ages and the overall number of preventive services that primary care is expected to deliver increases.
    Studies have shown that various health care personnel can increase preventive services used in primary care. For example, FOBT screening rates increased substantially when nurses were given responsibility for ordering FOBT.27 Well-trained nurse practitioners and physician assistants have been shown capable of safely and effectively performing flexible sigmoidoscopy.2830 A recent study11 documented the effectiveness of telephone counseling delivered by preventive care managers in increasing rates of breast, cervical, and CRC screening among low-income women. One evaluation of the use of tools (e.g., prevention checklists, computer monitoring, availability of services), teamwork (i.e., the division of labor within the practice and how the team worked together), and tenacity (i.e., the importance placed on preventive services by 1 or more members of the practice) identified teamwork and tenacity as especially influential in preventive services delivery in primary care settings.31
    Research gaps. Despite research support for the team approach to delivering CRC screening, adoption has been limited. Although growth in the supply of nonphysician primary care clinicians has been rapid,24 information on the extent to which team members other than the primary care physician are involved in CRC screening delivery is sparse. In a national survey conducted in 1999–2000, one-quarter of primary care physicians reported using a nurse practitioner or physician assistant to provide screening with FOBT. Few physicians, however, reported using these providers to perform colorectal endoscopy procedures.32 These findings need to be updated and to incorporate information from advanced practice nurses who may provide preventive care independent of physicians. Further, whereas numerous studies have shown that a recommendation for CRC screening from the primary care physician is a particularly powerful facilitator, it is unknown whether other team members are perceived by patients as equally credible advisors. Colonoscopy rates are increasing relative to other CRC screening tests,33 and there is concern that this will strain capacity. More research is needed to assess the ability of providers other than gastroenterologists and surgeons to safely and effectively perform this procedure. Finally, further study of primary care physicians’ attitudes toward team-based care is warranted given recent findings from a national survey indicating that one-third of primary care physicians believe “the team process makes care more cumbersome”.34
  • Advanced information systems.
    What is known. Electronic health records (EHRs), considered the central nervous system of the New Model of Primary Care, are crucial because they improve the practice’s ability to systematically identify and track patients for various risks and services.15,16,22 Such systems can identify those eligible for CRC screening, facilitate the use of reminder and recall systems, and enable monitoring of screening utilization, delivery, and outcomes for purposes of performance measurement and quality improvement. Reminder systems, audit, and feedback have all been shown effective in improving screening practice.22,35,36 The New Model assumes that information systems will be user friendly and appropriate for busy practices and allow all team members to review and exchange patient data related to screening, thereby making collaboration and communication easier.
    Research gaps. Despite growing evidence about EHRs, adoption of information technologies by primary care practices has been slow. Recent data show that less than one-quarter of primary care physicians use EHRs routinely or occasionally; less than half send patients computerized or manual reminder notices about preventive or follow-up care, and few e-mail patients routinely or occasionally.34,37 Moreover, 1 systematic review concluded that additional research is needed to identify ways of using information technology to reduce demands on appointment face-to-face time in primary care.38 For practices lacking EHRs, hand-held computers,39 or other information technology support, the electronic preventive services tracking system (i.e., Patient Electronic Care System) developed for the Bureau of Primary Care, Health Resources and Services Administration (http://www.cpca.org/healthcollabs/documents/PECS_info_packet.pdf), may be useful for efficiently and effectively delivering preventive care, including CRC screening.
  • Patient-centered care.
    What is known. In the New Model of Primary Care, patients are recognized as active participants in their own health care. Information technology advances are helping to transform patients’ roles by empowering them to make decisions about prevention and treatment. In particular, the availability of decision aids to inform patients of CRC screening options may enhance patient–physician screening discussions. Decision aids can improve knowledge, foster realistic expectations, and promote active participation in the decision-making process.40 It has been shown that recommended test options for CRC screening differ in ways that matter to patients—in effectiveness, convenience, safety, availability, and cost41,42—and that patient preferences for making decisions about CRC screening are heterogeneous.43 Some evidence suggests that practices can achieve higher screening rates by allocating adequate time to preventive services discussions.4447 In contrast, practices that do not ascertain patient preferences and instead offer just 1 approach to CRC screening may not realize high screening rates.48,49
    Research gaps. One systematic review of cancer screening studies, however, concluded that “current evidence is insufficient to determine the effectiveness of informed decision-making interventions for individuals in health care settings, for community members outside of health care settings, or for interventions targeted to health care systems and providers”.50 Specifically, it is unknown whether actively involving patients in a discussion of the factors for and against each test option increases CRC screening rates. Whereas discussions about CRC screening are more likely to occur during preventive care visits,51 most patient visits are for acute rather than preventive care.52 Such acute care visits very likely afford a less optimal venue for conversations about CRC screening. This is compounded by lack of reimbursement for health maintenance visits by the Medicare program, with the exception of a one-time “Welcome to Medicare” visit for new Medicare Part B enrollees. Thus, there is a need for studies of providers’ use of informed decision making for CRC screening in the context of different types of patient visits. Also, given the wide variability in costs of the recommended CRC screening tests and increased requirements for patient cost-sharing, there is need for research examining the influence of out-of-pocket costs on patients’ willingness to undergo CRC screening, their choice of screening tests, and providers’ propensity to offer screening.41
  • Improved efficiency and quality of services.
    What is known. For primary care practices to become more quality and cost accountable, they will require system supports and redesigned, more functional offices. For CRC screening, mechanisms will be required to routinely and consistently recruit eligible patients and monitor outcomes, including adherence. In addition, the effectiveness of identifying and screening those at high risk can be increased through the use of systems that facilitate risk stratification based on family or personal history of adenomas or cancer and by clinical findings. Newer office systems will also be required to facilitate implementation of targeted and tailored interventions for subgroups of patients less likely to accept screening, especially those with low socioeconomic status, low literacy, or those who live in rural areas.
    Research gaps. Reviews22,35 have noted that organizational systems and practice-level interventions targeting providers and patients can increase screening rates. Although it is likely that several of the NCI/AHRQ-sponsored projects will show improvements in CRC screening delivery and quality, there is a need for more research to determine efficient and effective ways of “bundling” CRC screening with other routine preventive services. There also is need for more research in the community-based primary care settings where most U.S. adults receive their care rather than in academic-affiliated practices.
  • Enhanced practice finances.
    What is known. The New Model of Primary Care insists on an alternative to current, traditional fee-for-service financing of health care. By not providing practices with reimbursement for critical parts of the screening process (e.g., counseling about screening; tracking eligibility and test results), most current financing models for primary care have been barriers to screening. Under the New Model, practices would be fairly compensated for everything they do, including cognitive services and services that take place outside of the traditional provider–patient encounter, such as reminder contacts or communications by telephone or e-mail. In addition, the enhanced financial system would offer incentives for better performance, such as improved screening rates and tracking of eligible patients.
    Research gaps. Financing reform within the U.S. system remains a formidable challenge. Low reimbursement has been cited as a provider barrier to delivering CRC risk counseling and screening.5355 Use of sigmoidoscopy—a procedure historically performed by primary care physicians—is declining rapidly33,56,57; to what extent low reimbursement rates for performing the procedure may be contributing to the decline is unknown. FOBT rates have leveled off.33 Whether this trend will continue with the newer immunochemical tests—which are reimbursed at a higher rate than standard guaiac-based FOBT—requires further monitoring. It has been shown that greater levels of physician reimbursement are associated with higher rates of preventive services delivery.58 Moreover, there is interest in pay for performance (P4P) measures as a means of improving the quality of care, but study results to date have been mixed. Evidence for the effectiveness of P4P schemes in fostering improved delivery of cancer screening or other preventive services is needed.5963 The complexity of physician reimbursement methods and incentive design may help explain the lack of effect of proposed P4P strategies so far. In sum, there is a great need for more research on how reimbursement influences preventive services delivery, and whether payment systems redesign will provide incentive for primary care providers to improve delivery of these services.
  • Training opportunities.
    What is known. Under the New Model of Primary Care, both clinicians in training and those in practice will have the opportunity to gain background and skills in areas critical to higher quality care. Improved performance by clinicians and office staff in areas such as communication skills, cultural competence, use of information technology, and team/systems management could clearly impact the delivery of effective services, including CRC screening. Efforts are underway to improve the quality of care by focusing on residency training programs. The Accreditation Council for Graduate Medical Education has developed a new initiative emphasizing patient outcomes (http://www.acgme.org/outcome). Although CRC screening is not specifically mentioned in the initiative, it could be encouraged as an example of such core competencies as systems-based practice and practice-based learning and improvement.
    Research gaps. More efforts to design and evaluate primary care providers’ training needs related to CRC screening are warranted. Studies describing evaluations of the cancer prevention practices and continuing education needs of primary care providers are sparse64,65; such studies may have been done recently but are not in published sources. As noted by Sandy and Schroeder,24 training needs for primary care physicians under the New Model of Primary Care include communication skills, information technology, working in teams, and behavior change counseling. These skills are particularly relevant to and critical for the effective delivery of a complex preventive service like CRC screening. Moreover, interested clinicians may wish to gain skills in performing CRC screening procedures (e.g., endoscopy) as a means of making these services more available to their patients.
CRC screening is a particularly challenging preventive service to implement in primary care practice. Unlike most other preventive services, there are multiple test options, requiring patients and providers to discuss and select the approach that is most appropriate for, and acceptable to, the patient. There also are procedural complexities. CRC screening is perhaps unique among preventive services in the level of effort required of patients to successfully complete screening. For example, fecal occult blood testing may require dietary restrictions and multiple stool samples, whereas sigmoidoscopy and colonoscopy entail rigorous cleansing of the colon. The use of intravenous sedation during colonoscopy also requires patients to identify someone who can accompany them home post-procedure. These factors combined with unique features of the patient, provider, practice setting, and external environment may explain in part why CRC screening continues to be underutilized.
By increasing CRC screening rates in the United States, substantial reductions in CRC mortality would be realized.66 Improvement in CRC screening rates is achievable largely through the efforts of primary care practices to implement effective systems and procedures for screening delivery. Within the framework of a New Model of Primary Care, we described evidence-based strategies for provision of CRC screening by primary care practices, and an active, innovative research portfolio that NCI and AHRQ have developed to identify effective new strategies. In particular, studies funded under the NCI/AHRQ initiative will contribute new knowledge about 4 elements of the New Model: team approach to care delivery, advanced information systems, patient-centered care, and improved efficiency and quality of services.
Although progress is evident, much remains to be done, as the challenges of providing services in the context of primary care are very real. As Frame has noted, “an ounce of prevention is a ton of work” (P. Frame, personal communication, June 29, 2006). Clinicians who desire more information about practice redesign and the New Model can go to a Web site developed by the American Academy of Family Physicians: http://www.transformed.com. Whereas this paper has focused on the primary care practice setting, numerous factors at other levels impact the processes of care delivered in individual practices.17 For example, public policy at the national and state levels can have powerful influence on whether and to what extent certain procedures and services are reimbursed. Both public policy and standards developed by professional organizations can enable or inhibit the provision of services by various provider types or teams. All sectors at many levels, including federal and state policy makers, professional organizations, and local communities, must recognize their roles and responsibilities in fostering and supporting the efforts of primary care providers to deliver responsive and viable preventive services. Only through the active engagement and support of primary care practices will the enormous potential of CRC screening be realized.
Acknowledgments
Financial Support and Disclosure Funding support for this review was provided by the National Cancer Institute and the Agency for Healthcare Research and Quality.
Potential Financial Conflicts of Interest None disclosed.
Appendix A
Table 1
Table 1
Appendix A. NCI and AHRQ Funded Studies: Colorectal Cancer Screening in Primary Care Practice
Appendix B
Table 2
Table 2
Appendix B. Participants in Improving Colorectal Cancer Screening Delivery, Utilization, and Outcomes: the State of the Science
1. Walsh JM, Terdiman JP. Colorectal cancer screening: scientific review. JAMA. 2003;289:1288–96. [PubMed]
2. Smith RA, Cokkinides V, von Eschenbach AC, et al. American Cancer Society guidelines for the early detection of cancer. CA Cancer J Clin. 2002;52:8–22. [PubMed]
3. U.S. Preventive Services Task Force. Screening for colorectal cancer: recommendation and rationale. Ann Intern Med. 2002;137:129–31. [PubMed]
4. Winawer SJ, Fletcher RH, Miller L, et al. Colorectal cancer screening and surveillance: clinical guidelines and rationale-updated based on new evidence. Gastroenterology. 2003;124:544–60. [PubMed]
5. Shea S, DuMouchel W, Bahamonde L. A meta-analysis of 16 randomized controlled trials to evaluate computer-based clinical reminder systems for preventive care in the ambulatory setting. J Am Med Inform Assoc. 1996;3:399–409. [PMC free article] [PubMed]
6. Snell JL, Buck EL. Increasing cancer screening: a meta-analysis. Prev Med. 1996;25:702–7. [PubMed]
7. Vernon SW. Participation in colorectal cancer screening: a review. J Natl Cancer Inst. 1997;89:1406–22. [PubMed]
8. Balas EA, Weingarten S, Garb CT, et al. Improving preventive care by prompting physicians. Arch Intern Med. 2000;160:301–8. [PubMed]
9. Peterson SK, Vernon SW. A review of patient and physician adherence to colorectal cancer screening guidelines. Semin Colon Rectal Surg. 2000;11:58–72.
10. Pignone M, Harris R, Kinsinger L. Videotape-based decision aid for colon cancer screening. A randomized, controlled trial. Ann Intern Med. 2000;133:761–9. [PubMed]
11. Dietrich AJ, Tobin JN, Cassells A, et al. Telephone care management to improve colorectal cancer screening among low-income women: a randomized, controlled trial. Ann Intern Med. 2006;144:563–71. [PubMed]
12. Klabunde CN, Riley GF, Mandelson MT, et al. Health plan policies and programs for colorectal cancer screening: a national profile. Am J Manag Care. 2004;10:273–9. [PubMed]
13. Yarnall KSH, Pollak KI, Ostbye T, Krause KM, Michener L. Primary care: is there enough time for prevention? Am J Public Health. 2003;93:635–41. [PubMed]
14. Kroenke K. The many c’s of primary care. J Gen Intern Med. 2004;19:708–9. [PMC free article] [PubMed]
15. Martin JC, Avant RF, Bowman MA, et al. The Future of Family Medicine: a collaborative project of the family medicine community. Ann Fam Med. 2004;2(Suppl 1):S3–32. [PubMed]
16. Larson EB, Fihn SD, Kirk LM, et al. The future of general internal medicine. Report and recommendations from the Society of General Internal Medicine (SGIM) Task Force on the Domain of General Internal Medicine. J Gen Intern Med. 2004;19:69–77. [PMC free article] [PubMed]
17. Zapka JG, Taplin SH, Solberg LI, Manos MM. A framework for improving the quality of cancer care: the case of breast and cervical cancer screening. Cancer Epidemiol Biomark Prev. 2003;12:4–13.
18. Greco PJ, Eisenberg JM. Changing physicians’ practices. New Eng J Med. 1993;329:1271–4. [PubMed]
19. Robertson N, Baker R, Hearnshaw H. Changing the clinical behavior of doctors: a psychological framework. Qual Health Care. 1996;5:51–4. [PMC free article] [PubMed]
20. Grimshaw JM, Eccles MP, Waler AE, Thomas RE. Changing physicians’ behavior: what works and thoughts on getting more things to work. J Contin Educ Health Prof. 2002;22:237–43. [PubMed]
21. Davis DA, Thomson MA, Oxman AD, Haynes B. Changing physician performance: a systematic review of continuing medical education strategies. JAMA. 1995;274:700–5. [PubMed]
22. Stone E, Morton SC, Hulscher ME, et al. Interventions that increase use of adult immunization and cancer screening services: a meta-analysis. Ann Intern Med. 2002;136:641–51. [PubMed]
23. Litaker D, Flocke SA, Frolkis JP, Stange KC. Physicians’ attitudes and preventive care delivery: insights from the DOPC study. Prev Med. 2005;40:556–63. [PubMed]
24. Sandy LG, Schroeder SA. Primary care in a new era: disillusion and dissolution? Ann Intern Med. 2003;138:262–7. [PubMed]
25. Landon BE, Reschovsky J, Blumenthal D. Changes in career satisfaction among primary care and specialist physicians, 1997–2001. JAMA. 2003;289:442–9. [PubMed]
26. Moore G, Showstack J. Primary care medicine in crisis: toward reconstruction and renewal. Ann Intern Med. 2003;138:244–7. [PubMed]
27. Thompson NJ, Boyko EJ, Dominitz JA, et al. A randomized trial of a clinic-based support staff intervention to increase the rate of fecal occult blood test ordering. Prev Med. 2000;30:244–51. [PubMed]
28. Maule WF. Screening for colorectal cancer by nurse endoscopists. N Engl J Med. 1994;330:183–7. [PubMed]
29. Wallace MB, Kemp JA, Meyer F, et al. Screening for colorectal cancer with flexible sigmoidoscopy by nonphysician endoscopists. Am J Med. 1999;49:158–62.
30. Schoenfeld PS, Cash B, Kita J, Piorkowski M, et al. Effectiveness and patient satisfaction with screening flexible sigmoidoscopy performed by registered nurses. Gastrointest Endosc. 1999;107:214–8.
31. Carpiano RM, Flocke SA, Frank SH, Stange KC. Tools, teamwork, and tenacity: an examination of family practice office system influences on preventive service delivery. Prev Med. 2003;36:131–40. [PubMed]
32. Sansbury LB, Klabunde CN, Mysliwiec P, et al. Physicians’ use of nonphysician healthcare providers for colorectal cancer screening. Am J Prev Med. 2003;25:179–86. [PubMed]
33. Meissner HI, Breen N, Klabunde CN, et al. Patterns of colorectal cancer screening uptake among men and women in the United States. Cancer Epidemiol Biomark Prev. 2006;15:389–94.
34. Audet AM, Davis K, Schoenbaum SC. Adoption of patient-centered care practices by physicians: results from a national survey. Arch Intern Med. 2006;166:754–9. [PubMed]
35. Zapka JG, Lemon SC. Interventions for patients, providers, and health care organizations. Cancer. 2004;101(5 Suppl):1165–87. [PubMed]
36. Jamtvedt G, Young JM, Kristoffersen DT, et al. Audit and feedback: effects on professional practice and health care outcomes. Cochrane Database Sys Rev. 2003;(3):CD000259.
37. Grant RW, Campbell EG, Gruen RL, et al. Prevalence of basic information technology use by U.S. physicians. J Gen Intern Med. 2006;21:1150–5. [PMC free article] [PubMed]
38. Jimbo M, Nease DE, Ruffin MT, et al. Information technology and cancer prevention. CA Cancer J Clin. 2006;56:26–36. [PubMed]
39. Price M. Can hand-held computers improve adherence to guidelines? A pilot study of family doctors in British Columbia. Can Fam Physician. 2005;51:1506–7. [PMC free article] [PubMed]
40. O’Connor AM, Stacey D, Entwistle V, et al. Decision aids for people facing health treatment of screening decisions. Cochrane Database Sys Rev. 2003;(2):CD001431.
41. Pignone M, Bucholtz D, Harris R. Patient preferences for colon cancer screening. J Gen Intern Med. 1999;14:432–7. [PMC free article] [PubMed]
42. Dolan JG. Patient priorities in colorectal cancer screening decisions. Health Expect. 2005;8:334–44. [PubMed]
43. Messina CR, Lane DS, Grimson R. Colorectal cancer screening attitudes and practices: preferences for decision making. Am J Prev Med. 2005;5:439–46. [PubMed]
44. Levy BT, Dawson J, Hartz AJ, et al. Colorectal cancer testing among patients cared for by Iowa family physicians. Am J Prev Med. 2006;31:193–201. [PubMed]
45. Greiner KA, Engelman KK, Hall MA, et al. Barriers to colorectal cancer screening in rural primary care. Prev Med. 2004;38:269–75. [PubMed]
46. Flocke SA, Stange KC, Zyzanski SJ. The association of attributes of primary care with the delivery of clinical preventive services. Med Care. 1998;36(Suppl 8):AS21–30. [PubMed]
47. Sontag SJ, Durczak C, Aranha GV, et al. Fecal occult blood screening for colorectal cancer in a Veterans Administration hospital. Am J Surg. 1983;145:89–94. [PubMed]
48. Ling BS, Moskowitz MA, Wachs D, et al. Attitudes toward colorectal cancer screening tests. J Gen Intern Med. 2001;16:822–30. [PMC free article] [PubMed]
49. Denberg TD, Melhado TV, Coombes JM, et al. Predictors of nonadherence to screening colonoscopy. J Gen Intern Med. 2005;20:989–95. [PMC free article] [PubMed]
50. Briss P, Rimer B, Reilley B, et al. Promoting informed decisions about cancer screening in communities and healthcare systems. Am J Prev Med. 2004;26:67–80. [PubMed]
51. Patel P, Forjuoh SN, Avots-Avotins A, et al. Identifying opportunities for improved colorectal cancer screening in primary care. Prev Med. 2004;39:239–46. [PubMed]
52. Stange KC, Zyzanski SJ, Jaen CR, et al. Illuminating the black box. A description of 4454 patient visits to 138 family physicians. J Fam Pract. 1998;46:377–89. [PubMed]
53. Fairfield KM, Chen WY, Colditz GA, et al. Colon cancer risk counseling by health-care providers: perceived barriers and response to an internet-based cancer risk appraisal instrument. J Cancer Educ. 2004;19:95–7. [PubMed]
54. Klabunde CN, Vernon SW, Nadel MR, et al. Barriers to colorectal cancer screening: a comparison of reports from primary care physicians and average-risk adults. Med Care. 2005;43:939–44. [PubMed]
55. Lewis JD, Asch DA. Barriers to office-based screening sigmoidoscopy: does reimbursement cover costs? Ann Intern Med. 1999;130:525–30. [PubMed]
56. Brown ML, Klabunde CN, Mysliwiec P. Current capacity for endoscopic colorectal cancer screening in the United States: data from the National Cancer Institute Survey of Colorectal Cancer Screening Practices. Am J Med. 2003;115:129–33. [PubMed]
57. Wigton RS, Alguire P. The declining number and variety of procedures done by general internists: a resurvey of members of the American College of Physicians. Ann Intern Med. 2007;146:355–60. [PubMed]
58. McInerny TK, Cull WL, Yudkowsky BK. Physician reimbursement levels and adherence to American Academy of Pediatrics well-visit and immunization recommendations. Pediatrics. 2005;115:833–8. [PubMed]
59. Rosenthal MB, Frank RG, Li A, et al. Early experience with pay-for-performance: from concept to practice. JAMA. 2005;294:1788–93. [PubMed]
60. Pourat N, Rice T, Tai-Seale M, et al. Association between physician compensation methods and delivery of guideline-concordant STD care: is there a link? Am J Manag Care. 2005;11:426–32. [PubMed]
61. Roski J, Jeddeloh R, An L, et al. The impact of financial incentives and a patient registry on preventive care quality: increasing provider adherence to evidence-based smoking cessation practice guidelines. Prev Med. 2003;36:291–9. [PubMed]
62. Wee CC, Phillips RS, Burstin HR, et al. Influence of financial productivity incentives on the use of preventive care. Am J Med. 2001;110:181–7. [PubMed]
63. Hillman AL, Ripley K, Goldfarb N, et al. Physician financial incentives and feedback: failure to increase cancer screening in Medicaid managed care. Am J Public Health. 1998;88:1699–701. [PubMed]
64. Nadel MR, Shapiro JA, Klabunde CN, et al. A national survey of primary care physicians’ methods for screening for fecal occult blood. Ann Intern Med. 2005;142:86–94. [PubMed]
65. Costanza ME, Hoople NE, Gaw VP, et al. Cancer prevention practices and continuing education needs of primary care physicians. Am J Prev Med. 1993;9:107–12. [PubMed]
66. Vogelaar I, van Ballegooijen M, Schrag D, et al. How much can current interventions reduce colorectal cancer mortality in the U.S.? Mortality projections for scenarios of risk-factor modification, screening, and treatment. Cancer. 2006;107:1624–33. [PubMed]
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