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standpoint. For women, screening begins 3 years after onset of sexual activity or by age 21 to look for precursors to cervical cancer, by age 40 for breast cancer, and by age 50 for colorectal cancer. Screening for men begins at age 50 for colon cancer; a discussion of prostate cancer should also occur at that time so that men understand the strengths and weaknesses of current knowledge.10

However, identifying the population at risk involves more than specifying gender or age range. It is also important to understand the cultural characteristics of populations, their interest in screening, and their understanding of screening tests so that those at risk understand the recommendations and seek the appropriate tests.104,156,157 Those at highest risk of late-stage cancers after screening are those who have not been screened before.155

Figure 24.2 shows that screening rates in the United States vary from as low as 10% of women having had a recent endoscopic evaluation of colorectal cancer to as high as 81% having had a recent Pap smear.158 The figure shows that, as of the year 2000, less than 30% of men or women had undergone FOBT within the previous 2 years, and fewer had undergone endoscopy. Men are more likely to report having had a PSA test than either FOBT or endoscopic screening.159 Because the potential mortality reduction among individuals screened for colon cancer is promising, encouraging CRC screening is becoming a high priority.10,160

Although Figure 24.2 demonstrates rising rates of mam-mographic screening and sustained cervical cancer screening, women with lower incomes are less likely to have access to care and are less likely to be screened for these two cancers, even though programs are in place to reach low-income women in all 50 states.161,162 Across the United States, an estimated 15% of individuals are without insurance coverage at any given time, and a much higher percentage is without coverage some time during the year.163 Lack of insurance and lack of a regular source of health care are highly correlated with lack of screening.158,164,165 For example, African-

Americans are less likely to have health insurance than Caucasians and are therefore less likely to undergo screening tests for CRC.162,166 It is estimated that cancer mortality is 19% higher in the lowest socioeconomic groups than in the highest.167 Recently, levels of cancer screening among racial minorities have improved to the point that they approach the levels of screening among Caucasians; people without health insurance or a regular source of health care continue to be underscreened.168 As a nation, we cannot achieve the maximum mortality reduction afforded by cancer screening if some populations go unscreened or untreated.

Identifying the Method of Recruitment

Reaching individuals, however, is not only a function of income and access. Even when they have access to care, not all people seek recommended screening.155,169,170 Providers may work with their teams, practices, health plans, third-party payers, and community to develop recruitment methods for screening. There is evidence that changes in practice that affect multiple levels of health care, including reimbursement, records systems, and tailoring of recruitment messages, have the strongest impact.171,172

Ultimately, practitioners must make choices about how to reach individuals with appropriate recommendations and encourage them to consider screening. This is a crucial step in the screening process; for example, a recommendation from a primary care physician is a primary predictor of whether women seek colorectal cancer screening.173 However, physicians' recommendations are not always consistent with screening guidelines; for example, a nationwide survey of primary care physicians suggested the presence of knowledge gaps and suboptimal screening delivery for CRC screening.160 Primary care physicians also face substantial time limitations with regard to making all necessary and appropriate screening recommendations in light of their other prevention and treatment obligations174; therefore, systematic changes may have the largest impact on making the screening recommendation.172

One key systematic change is the implementation of clinical reminder systems, as there is strong evidence that issuing reminders leads to increased screening rates for film-screen mammography and cervical cancer.172,175-178 The two major types of reminders are inreach and outreach. Inreach reminders involve notifying a provider that a patient is due for a screening test while he or she is in the office. Systems to provide inreach reminders may be as simple as a chart review and paper alert or as sophisticated as an electronic note on an automated medical record. Overall, inreach reminders and physician feedback have been shown to result in the mammography screening of an additional 5% to 20% of the study population compared with "usual care" con-trols.179 Outreach reminders consist of contacting individuals outside of an office visit. Studies involving telephone calls from a cancer registry, mailed recommendations, and motivational telephone calls addressing specific barriers to screening have shown that such reminders result in the Pap and mammography screening of an additional 15% to 31% of the study population compared with usual care.175,177

Even after recommendations are made, ensuring that individuals seek screening may require adopting and adapting new strategies to encourage women to follow through on the recommendation. For example, McPhee and colleagues have shown that having female lay leaders discuss screening at gatherings in women's homes promotes the use of film-screen mammography among Cambodians.180 Understanding factors that affect use of screening tests will help providers work with members of their organizations and communities to plan effective education and recruitment strategies for the populations they serve. The process of understanding and enabling individuals to manage their care has been called "self-management support" by some, and it may be critical to successful screening implementation.181

Clarifying the Screening Approach

In addition to ordering the screening test, the primary care provider may be responsible for conduct the screening. Organizing the care within a practice is therefore critical to getting screening accomplished. How that screening occurs, however, differs by the organizational setting of healthcare delivery, the cancer site, the set of screening tests recommended, and which test or set of tests the patient prefers. For example, screening mammography and colonoscopy depend upon referrals whereas cervical cancer screening, FOBT, and sigmoidoscopy can be conducted by the primary care team. To incorporate cancer screening into a busy practice, primary care providers need to organize their approach and clarify who is talking with the patient, what is being said, and how tests are ordered. This is all part of organizing the approach to screening, and it has been shown to increase screening rates when implemented systematically in practice using the entire healthcare team.172,182-184

Developing the Follow-Up Approach

When testing requires a referral, a tracking system to document the patient's progress through the care continuum can be helpful. The proportion of positive screening tests varies with the type of test but, in general, is about 10% (see Tables 24.1, 24.3, 24.5, 24.7). Follow-up for these individuals is not automatic, and failure to ensure successful follow-up compromises the mortality reduction achievable.178 For example, follow-up for positive FOBT has been estimated to range between 49% and 79%,185 and follow-up after a mammogram was as low as 35% women in one HMO even though access to care was assured.186 In a review of published evaluations of follow-up after positive screening tests, Yabroff and colleagues found that two-thirds of reported studies had follow-up rates below 75%.13 Among the 45 observational studies in her review, only 1 showed follow-up greater than 90%.13 Factors that improved follow-up of abnormal tests included addressing the lack of health insurance for a patient, using peer counselors, making system-wide changes in a health plan or clinic, and more actively encouraging patients to manage their care.13,172

Because of apparent problems with follow-up of abnormal tests, a framework has been outlined for thinking through the issues and developing methods to ensure follow-up of positive tests.13 Healthcare team members can use the work of Yabroff and others to guide their design of a system to ensure follow-up. Studies indicate that several elements are necessary for a successful follow-up system. First, a mechanism to ensure communication between the person performing the screening and the providers responsible for follow-up is necessary. Even if the provider conducts the test, as is usually the case with cervical cancer screening, clinicians need some method of ensuring that they receive the test results. Second, the provider team needs to have a plan for dealing with a positive result once it is received, because not all positive results need to be acted upon and the primary care provider is not always the responsible party. For example, radiology facilities are obligated by the MQSA to report mammography results to all women screened. Yet even in this case, a woman notified by the radiologist may not respond.

Communication with the patient about the follow-up plan is the next critical step in the implementation process. Such communication should clarify which tests are needed and what those tests involve for the patient. Research shows that communication from the provider to the patient about the importance of follow-up and the details about further workup will influence whether follow-up occurs.13,187 Women with fears of painful procedures or fatalistic views regarding cancer diagnosis are less likely to comply with follow-up rec-ommendations.13 As shown in Tables 24.1, 24.3, 24.5, and

24.7, evaluations needed after a positive test vary from repeating the test or ordering additional mammograms or colonoscopy to surgical consultation. Incorporating the patient into the care plan has become an important part of follow-up care and may increase adherence to the plan.13 For example, telephone contact addressing women's perceptions of the cervical cancer screening test and educating them before or after the Pap test through interactive discussion improved follow-up by 24% to 26%.178 Ultimately, improving follow-up requires the coordinated effort of providers, staff working with them, and patients.

Referring for Treatment

After developing the follow-up approach, the next critical step is ensuring that patients are referred to and receive appropriate specialty care. Referral to oncology specialists by primary care providers (PCPs) depends on some degree of coordinated care. Developing this coordination was highlighted in the National Cancer Policy Board's 1999 analysis as a key step toward improving the quality of America's health care. They concluded that optimal cancer care delivery should ensure, among other things, a "mechanism to coordinate services."188 Also, a committee of the Institute of Medicine selected care coordination as one of 20 "priority areas" requiring concerted effort if the nation's healthcare system is to be transformed.188 Literature is sparse regarding referral barriers relevant to screened cancers, but access and reimbursement for the uninsured are a clear challenge.162 However, difficulties are not confined to those traditionally considered underserved by the healthcare system. Access to quality cancer treatment in general is subject to numerous barriers, including patient characteristics such as old age, low SES,162 minority race or ethnicity,189 and lack of health insurance. Researchers studying older cancer patients concluded that patient preference is a "major determinant in the referral decisions of primary care providers." Another potential issue is that PCPs might be unaware of cancer treatment options available to seniors.190 Recent work raises questions regarding referral patterns and points out that the majority of patients are not seen by an oncologist who might help them with decisions.191

Although treatment options and systems are not a focus of this chapter, clinicians need to be mindful of the institutional and insurance barriers that may limit access. Successful referrals in any cancer patient depend on factors such as physician characteristics (e.g., specialty, training, experience, age), quality of patient-provider communication, and complexity and constraints of the current healthcare environment.188

Steps are being taken to improve the coordination of cancer treatment after a positive screening. A pilot project that tested the effects of patient navigators ("proactive patient advocates") on removing barriers to diagnosis and state-of-the-art treatment found the concept promising.192 At the public policy level, Congress passed legislation in 2000 to fill the "treatment gap" in the National Breast and Cervical Cancer Early Detection Program by giving states the option to extend Medicaid benefits to uninsured women diagnosed through the program.193 To date, the U.S. Department of Health and Human Services has approved proposals from 48 states and the District of Columbia to implement the act (CDC).

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