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Seminars in Oncology Nursing, Vol 21, No 4 (November), 2005: pp 252-259

OBJECTIVES:
To review criteria for mass cancer screening among asymptomatic populations and barriers to secondary prevention of breast, cervical, and colorectal cancers. To describe challenges to implementing theoretically based interventions to increase appropriate cancer screening, follow-up, and surveillance.

SECONDARY PREVENTION CANCER

VICTORIA L. CHAMPION
AND

OF

DATA SOURCES:
Published journal articles, text books, and epidemiologic reports.

CONCLUSION:
Interventions to increase breast, cervical, and colorectal cancer screening participation must be approached from a systems perspective that includes patient, health care provider, and health care system variables.

SUSAN M. RAWL

IMPLICATIONS PRACTICE:

FOR

NURSING

ECONDARY prevention is dened as the early detection and treatment of disease before signs or symptoms are apparent. The promotion of secondary prevention of cancer through appropriate screening of asymptomatic individuals will yield signicant decreases in cancer morbidity and mortality.1 The importance of cancer screening as secondary prevention was highlighted by a special panel held in Washington, DC in June of 2003.2 This article will review areas relevant to secondary prevention of cancer and discuss future directions for research.

S
S

Understanding the array of factors that impede progress in the secondary prevention of cancer is necessary to improve care. Nurses have an important role in decreasing morbidity and mortality from breast, cervical, and colorectal cancers.

CANCERS APPROPRIATE

FOR

SCREENING

From Indiana University School of Nursing, Indianapolis, IN. Victoria L. Champion, DNS, RN: Associate Dean for Research, Indiana University School of Nursing, Indianapolis, IN. Susan M. Rawl, PhD, RN: Assistant Professor., Indiana University School of Nursing, Indianapolis, IN. Address correspondence to Victoria Champion, DNS, RN, Indiana University School of Nursing, 1111 Middle Dr, Indianapolis, IN 46202; e-mail: vchampio@ iupui.edu.

2005 Elsevier Inc. All rights reserved. 0749-2081/05/2104-$30.00/0 doi:10.1016/j.soncn.2005.06.007

creening asymptomatic individuals for cancer is appropriate only when there is evidence that screening will result in decreased morbidity or mortality. Cancers for which screening is appropriate have several characteristics.3 First, the cancer must present a clear threat to morbidity and mortality if gone undetected. Second, the cancer must have a preclinical phase that has a high prevalence and incidence as well as a natural history and biology that can be predicted. That is, the cancer must occur frequently enough and be present at a signicant rate for screening an asymptomatic population to make sense. Third, effective treatment for early stage cancer must be available so that early discovery of a cancer leads to treatment that will decrease mortality from the disease. Fourth, the screening test must be accessible and acceptable to both patients and health care providers so that adherence to screening can be achieved. Finally, the test should be able to be delivered to an asymptomatic population in a costeffective manner. Two characteristics are essential for a good screening test: specicity and sensitivity. If a test is sensitive it will be able to detect a specic cancer within a population. Sensitivity is important so that a test will actually nd most cases of cancer if they exist. A screening tests failure to discover a cancer early can result in late-stage disease and death. If a cancer screening test has high

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specicity, the test would have few false-positive results (ie, would not indicate a person had cancer if they were disease-free). A false-positive can create anxiety by identifying a person as having cancer when in fact they are cancer-free. The issue of false-positives becomes very important when considering patient anxiety and costs for extra medical procedures. Bastani et al discuss the negative psychological sequelae that can occur following receipt of an abnormal screening result.4 Initial responses to abnormal results are often associated with anxiety and intrusive thoughts. Researchers also have found lingering psychological symptoms present in many women when false-positive results occur.5,6 Other potential harm or negative consequences can result from population screening and the degree of this harm should be weighed against the potential gain. For instance, although rare, a screening colonoscopy could potentially result in a perforated colon, requiring immediate surgery. Thus, both sensitivity and specicity must be considered before screening is implemented in an asymptomatic population. Although there are several generally accepted criteria for screening asymptomatic people, the primary consideration is that a cancer screening test can effectively decrease morbidity and mortality from a site-specic cancer. However, the cost/benet ratio of screening is also considered. Currently, only three cancers are generally accepted as appropriate for asymptomatic and population-based screening based on scientic research: cervical cancer, breast cancer, and colorectal cancer. Scientic evidence of mortality benet for breast and colorectal cancer screening has been found through randomized controlled trials, which offer the best evidence of mortality benet for a screening test. Support for cervical cancer screening surfaced and was implemented before the recognized need for a randomized controlled trial. In the United States, cervical cancer rates are relatively low, primarily because of high participation in Papanicolaou (Pap) smear testing and subsequent early detection of cervical cancer. The incidence of cervical cancer in the United States between 1996 and 2000 was 9.6 cases /100,000. Deaths occurred in 3/100,000 women. Invasive cervical cancer has shown a signicant decrease since 1950, thought to be primarily because of the use of the Pap test.7 Case control studies have found mortality decrease with Pap smears.5,6,8 In-

cidence of and mortality from cervical cancer, however, vary greatly by race. The incidence for African American women is 12.4 per 100,000 versus only 9.6 among white women. Death rates among African American women are approximately double that of white women (5.9/100,000 v 3/100,000). There are no known physical risks associated with Pap smears. False-positive results are fairly common and can result in anxiety for those women, but methods to improve sensitivity and specicity are ongoing.9 It is estimated that almost 213,000 cases of breast cancer will be diagnosed in the United States in 2005 and there will be close to 41,000 deaths.10 Mammography screening has been shown by randomized controlled trials to decrease mortality from breast cancer. Almost two decades of studies have shown that breast cancer mortality can be decreased by 30% to 40% in women over 50.11-13 Although the mortality data for women aged 40 to 50 are less convincing, a meta-analysis of prospective data showed a signicant mortality reduction for screened women in this age group.14-16 Risk inherent in mammography screening includes anxiety from false-positives, discomfort or pain with the procedure, and potential radiation risk.17 The sensitivity of mammography is estimated at approximately 85% and most published screening guidelines recommend regular clinical breast examinations in addition to annual mammography.10,18,19 Approximately 105,000 cases of colorectal cancer are expected to occur in the United States in 2005, with almost 57,000 deaths. Both the incidence and death rates for African American men and women exceed those of their white counterparts. Between 1996 and 2000, 64 per 100,000 cases of CRC were found in white men compared with 72.4 per 100,000 in African American men. For females, the rate in Caucasians was 46.2 per 100,000 and in African Americans was 56.2. The death rates were 25.8 per 100,000 for white males and 34.6 per 100,000 for African American males. For females, white women had a rate of 17.5 per 100,00 compared with the rate of 24.6 among African American women. Recent studies have shown the effectiveness of screening in reducing CRC incidence and mortality.20-28 Randomized trials have shown that screening with fecal occult blood tests (FOBT) reduces mortality by over 30%.22,25,26 This reduction is achieved, in part, because FOBT leads to endoscopic screening with exible sigmoidoscopy

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or colonoscopy. Risks associated with CRC screening can include anxiety from false-positives as well as, very rarely, perforation of the colon. Distinct Stages of Secondary Prevention Risk assessment. Cancer screening is often considered only in relation to population adherence to accepted recommendations. To fully appreciate the benets of cancer screening, however, secondary prevention should be conceptualized as having ve distinct steps: (1) risk assessment, (2) appropriate screening, (3) diagnostic follow-up for abnormal screens, (4) appropriate treatment, and (5) appropriate surveillance. Because screening recommendations may be risk-based, an accurate assessment of individual risk is necessary before recommending specic screening tests. Risk assessment variables include identication of individual, family, lifestyle, and environmental factors that apply to an individual in relation to particular cancers. Risk assessment should include age, personal and familial history of cancers, and lifestyle factors that may protect or predispose an individual to a certain cancer. Gail and Rimer29 have published risk-based recommendations for breast cancer screening for women in their 40s. For colorectal cancer screening, risk assessment is imperative given the diversity of screening options available. For instance, a 55-year-old man whose father was diagnosed with colorectal cancer before age 60 is considered to be at increased risk for developing the same disease. Published guidelines indicate that this individual should be screened immediately with colonoscopy. Another individual of the same age but without a family history is at average risk and could be counseled to have an FOBT and sigmoidoscopy. Zapka et al30 discuss issues related to primary and secondary prevention in individuals who have been determined at high risk for certain cancers. Once a person is identied, risk-appropriate screening may be only the rst step. With emerging information about the effectiveness of chemopreventive agents and lifestyle modications, high risk individuals may need more than screening. Information about chemopreventive agents and lifestyle modications may be an important component of complete care. It might also be important to involve family members because their cancer risk may also be higher than average. With the increasing ability to identify genetic markers that predispose an individual to cancer, cancer genetic counseling and, in some cases, genetic testing

should also be considered. Therefore, a higher than average risk assessment should lead to a variety of considerations that include, but are not limited to, cancer screening. Appropriate screening. After determining the appropriate screening test, individuals must be convinced to complete the screening. Poor adherence to recommended screening tests remains a challenge for researchers and health care providers. Cervical cancer screening has shown the greatest adherence with 84% of non-Hispanic Caucasian women over 18 having had a Pap test within the past 3 years.31 However, adherence rates among Hispanic, American Indian, and Asian women, as well as recent immigrants, continue to be unacceptably low. Adherence to regular breast cancer screening is increasing, but we still have a ways to go. For all eligible women, 70.3% have had a mammography in the last 2 years but only 55.3% in the last year. Colorectal cancer screening remains our greatest challenge. Only 17.3% of eligible men or women have had an FOBT in the last year and 30% have had endoscopy (sigmoidoscopy or colonoscopy) within the past 5 years.32 Intervention strategies to increase cancer screening adherence have been reviewed by Zapka and Lemon.33 The last two decades have yielded intervention research directed at patients, providers, and health care organizations. Barriers have been identied at the health care setting level that include public policy such as lack of insurance and inadequate reimbursement for providers. Organizational barriers can include lack of available resources for screening and prohibitive waiting time or ofce hours. Providers often cite lack of time to discuss preventive care, lack of reimbursement, and inadequate knowledge about optimal screening methods. Patient barriers have included lack of assessed risk for getting cancer, inadequate knowledge and perception of the benets of screening, the pain of a procedure, and lack of time to make appointments. One barrier that has been consistently identied is lack of provider recommendation. Future intervention research should build on what we currently know and several factors should lead future research. One such factor is the need to consider multilevel approaches to interventions.3,34 Most intervention studies have studied patients, providers, or systems in isolation from each other. An integrated approach is necessary to maximize intervention effect. Second,

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the operational denition of screening behaviors often differs across studies. When adherence to colorectal cancer screening is measured differently across intervention studies for example, outcomes are difcult to compare. Rakowski and Breslau35 describe the need to identify interventions that best promote continued screening as well as eliminating the disparity in screening rates across cultures and genders. We also need to consider the interrelationships between cancer screening and other health behaviors. Much of the screening research has occurred in women through intervention trials to increase cervical and breast cancer screening. With the advent of population-based screening for colorectal cancer, interventions need to be tested in both men and women. More studies need to consider the costeffectiveness of strategies and the minimal interventions needed to promote screenings across subgroups. Advancing technology in particular presents new opportunities for renement of interventions to promote cancer screening.36-38 Computer-generated health communication interventions have emerged as a promising strategy for inuencing health beliefs, attitudes toward screening, and screening behaviors. Tailored interventions are dened as any combination of information and behavior change strategies intended to reach one specic person, based on characteristics that are unique to that person, related to the outcome of interest, and derived from individual assessment.39 Tailoring refers to a process of creating individualized interventions that use demographic and psychosocial data collected from each person to generate customized feedback to meet his or her unique needs.40,41 Individually tailored health communications can be delivered using a variety of media, but interactive computer programs hold particular promise. Finally, with rapid development of new screening technologies, behavioral scientists need to be involved at the beginning to identify components of patient acceptance and uptake of new screening strategies. Diagnostic follow-up for abnormal screens. Mass screening of asymptomatic individuals can result in abnormal or questionable results requiring diagnostic follow-up to determine if a cancerous lesion is indeed present. The follow-up of abnormal results has received little attention, yet follow-up is critical to decreasing mortality and morbidity.4 Yarbroff et al42 found that over 25% of patients with abnormal cancer screening ndings

failed to receive appropriate follow-up care. For cervical, breast, and colorectal cancer, the denitions of abnormal results vary as does recommended follow-up.4 Interventions to increase follow-up care have been targeted to patients, but little research has focused on providers and health care systems.4 Several issues must be addressed when considering abnormal ndings. First, standardized denitions of an abnormal screening and appropriate follow-up are needed. Second, we must identify the patient, provider, and system barriers to appropriate and timely follow-up. Third, we must identify and address the impact that an abnormal cancer screen can have on patients and their future behavior. Some patients who have endured unnecessary and expensive diagnostic evaluation may be less willing to participate in continued regular screening in the future. Finally, research that addresses follow-up for abnormal screening needs to address validity of data collection and denitions of appropriate follow-up. Appropriate treatment. Following denitive diagnosis of a preclinical lesion, appropriate treatment must be procured. For an abnormal Pap smear, colposcopy is often indicated. If a breast biopsy determines a malignancy is present, a systematic evaluation and treatment plan are completed. All abnormal colorectal cancer screening results requires further diagnostic testing but the recommendations for follow-up varies depending on the screening test. A positive FOBT should always be followed by complete examination of the colon via colonoscopy. However, recent data indicate that this is often not done.43 A systematic diagnostic work-up is indicted when a large adenomatous polyp is found during a colonoscopy. Zapka et al30 identify gaps in the process of care that can result in a late-stage cancer diagnosis. First, the initial cancer may have been missed by a test that was not sensitive enough to detect disease. Second, even if an abnormal result is found, the patient may not receive appropriate follow-up care. Problems can occur with communication to the physician regarding abnormal results. Mistakes can occur when patients are not notied of abnormal results. Most frequently, however, patients do not follow-up when informed of abnormal results because they do not understand the importance of additional testing or for other reasons. Appropriate surveillance. Patients who have been treated for cancer need periodic surveillance

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for both the cancer that was originally diagnosed and for any secondary cancers that may develop. Depending on the cancer type, stage, and treatment, some patients may be put on more frequent surveillance and recall than those who have not had a cancer diagnosis. It is important for the oncologist to determine if follow-up should occur through his or her ofce or be referred back to a local physician. All too often this decision is not made, leaving the patient to decide when and where follow-up visits should occur.

THEORETICAL PERSPECTIVES
heories can provide guidance for predicting individual adherence to cancer screening as well as guidance about the necessary processes for delivery of care.30 Behavioral theories have provided guidance in many intervention studies to increase adherence to cancer screening guidelines. Theories such as the Health Belief Model (HBM) and The Transtheoretical Model (TTM) have allowed us to tailor interventions to individuals using new technologies.44 The Health Belief Model (HBM) The HBM provides guidance for tailoring messages according to beliefs shown to inuence screening. Two of its constructs (perceived benets and barriers related to a specic action) correspond with the pros and cons of the TTMs decisional balance construct. Most studies have found signicant correlations between perceived benets and barriers, respectively, and mammography use.45-50 In addition to perceived benets and barriers, the HBM includes the concepts of perceived risk of contracting the health problem51-53 and condence in the ability to take an action (self-efcacy). Several studies have found perceived risk to be positively related to mammography use.45-47,54-57 Self-efcacy, added to the original HBM as an inuence on health behavior,53 has shown promise as an important predictor of mammography screening. Similarly, perceived benets and barriers to CRC screening were recently reported as signicantly related to FOBT, sigmoidoscopy, and colonoscopy.58,59 The Transtheoretical Model (TTM) According to Prochaska and Velicer,60 health behavior change can be viewed on a continuum wherein the individual moves from not consider-

ing an action or health behavior to maintaining adoption of the behavior. The model considers the individuals past history of the targeted behavior and intention regarding future behavior. Decisional balance is dened as the assessment by an individual of the benets (pros) of a health action relative to the barriers (cons). As mentioned, these pros and cons correspond to the HBMs concepts of perceived benets and barriers (see below). Changing or initiating a health action involves a gradual change in decisional balance. The TTM has been applied to mammography screening and has guided a number of effective mammography interventions,61-63 including intervention trials conducted by the authors.57,63,64 The TTM has also been supported in the context of CRC screening.65 In our intervention research, we attempt to inuence decisional balance through tailored messages designed to increase perceived benets and decrease perceived barriers to specic screening tests that are endorsed by the individual intervention recipient. We use the TTM to guide development of messages tailored to each recipients stage of mammography or colorectal screening adoption. The denitions and validation of mammography stage have been consistent across several studies.66-68 Criteria for dening stage of adoption for breast cancer are consistent with the National Cancer Institutes consortium stage denitions and were used to develop colorectal stage denitions. Other researchers have addressed system issues through broader theories. Zapka and Lemon33 address the entire continuum of care from risk assessment to surveillance when presenting the Continuum of Cancer Care model. The processes of care are identied, as well as challenges that occur anywhere throughout the continuum. Furthermore, different levels are considered, from the individual patient to the health care system to the community. The interrelationships of organizational factors, screening test characteristics, and patient and provider variables are discussed in the following section. Other models often used to address issues at the organizational and community level are the PRECEDE-PROCEED Model and the Behavioral Model of Utilization.69,70 Both models emphasize the importance of multiple factors, including individual, family, health care system, and community factors. Many interactions along the continuum of care are required for optimal cancer screening and follow-up. Key to all processes are open lines of communication. Indeed, Zapka and

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Lemon33 describe many failures that occur when communication cycles are broken. For instance, failure to notify a patient of an abnormal screening result could lead to delayed treatment. Green and Krueter,69 following the Behavioral Model of Utilization, emphasize predisposing, enabling, and reinforcing factors at the individual and macro level. Predisposing factors include knowledge and beliefs about screening from both the patient and provider perspective. Enabling factors are related to the health care system and include such things as resources and reimbursement levels. Reinforcing factors include public, community, and provider norms. Invasive cancers can result when there are breakdowns anywhere during the processes of care. Challenges We are faced with many challenges in the attempt to provide optimal levels of secondary prevention particular for cancers, including cervical, breast, and colorectal. A thorough review of the array of challenges is described by Meissner et al.3 Four broad areas likely to have the greatest impact on secondary prevention include: (1) development of new technologies for screening; (2) a multilevel approach that considers the interrelationships of individual, provider, health care system, and community; (3) consideration of methodologic problems that occur in current interventions; (4) identifying the most cost-effective methods of screening and interventions to increase screening; and (5) dissemination of effective cancer screening interventions. In relation to new technologies, cancer screening tests are continually evolving and changing. Basic science is quickly identifying genetic and molecular characteristics related to the development of certain cancers. The future may allow us to identify a subset of individuals who are likely to develop a cancer and target only this subset for screening. Meissner et al3 advocate addressing the behavioral issues related to dissemination of tests before their development. The second critical need is development of effective systems approaches to fully address all issues related to secondary prevention. Zapka et al30 present a process of care model that considers individual, provider, health care system, and community interventions. The Institute of Medicine emphasizes the need to consider interventions that address the individual as well as macro level

concerns.71 Solberg et al72,73 advocate a systems approach to delivering preventive services. Most important in relation to methodologic problems in this eld is the development of consensus about screening guidelines, denitions of abnormal results, denitions of adherence, and recalls after abnormal results. Inherent in these concerns are complex issues that are not easily addressed. For instance, many research studies have relied on self report use of screening tests, which may or may not be reliable. Organizations often present conicting screening guidelines or fail to dene adherence. A good example was the conict about mammography recommendations that occurred in the 1990s. Currently, the recommendations for colorectal cancer screening are complex, confusing, and consistently being revised . Fourth, any intervention to encourage adherence to screening must be cost-effective in our health care system. The challenge is to develop sensitive, specic, and acceptable cost-effective screening tests and strategies. Finally, dissemination must occur before the true benets of secondary prevention efforts are realized. Glasgow et al74 identify four issues that affect dissemination into practice.74 The rst is that dissemination will not occur naturally. Research on the diffusion of clinical research found it took 17 years to apply just 14% of research ndings to clinical practice.74,75 Second, standardization of reporting of research results must be achieved before the evidence base for effective outcomes can be determined. Third, dissemination must be considered when designing interventions. The most effective intervention is only as good as its ability to be used in clinical practice. Fourth, barriers to dissemination can arise in four areas: (1) characteristics of the intervention, (2) characteristics of the research design, (3) characteristics of the potential adoption settings, and (4) interactions among the other three barrier types. The rst area reects difculties in using the intervention such as cost, appeal to users, and difculty in use. The second area relates to the relevance of the research to patients, clinicians, or settings. Characteristics of the adoption settings could include prevailing practices of clinicians, resistance to change, and high demands. Glasgow et al74 suggest that theories or models should guide dissemination research. Examples include Rogers Diffusion of Innovations theory, which addresses issues related to effective dissemination.76 The impact of cancer screening on mor-

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bidity and mortality will be directly related to the number of individuals who obtain initial screening, appropriate follow-up, treatment when necessary, and continued lifetime surveillance. Re-

search is needed to determine how to most costeffectively achieve all these steps and how to efciently disseminate results of intervention trials into clinical practice.

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