Organizational Factors and the Cancer Screening Process

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1 DOI: /jncimonographs/lgq008 The Author Published by Oxford University Press. All rights reserved. For Permissions, please Organizational Factors and the Cancer Screening Process Rebecca Anhang Price, Jane Zapka, Heather Edwards, Stephen H. Taplin Correspondence to: Rebecca Anhang Price, PhD, SAIC-Frederick, Inc., Applied Cancer Screening Research Branch, Division of Cancer Control and Population Sciences, National Cancer Institute, 6130 Executive Blvd, EPN 4103A, Rockville, MD ( Cancer screening is a process of care consisting of several steps and interfaces. This article reviews what is known about the association between organizational factors and cancer screening rates and examines how organizational strategies can address the steps and interfaces of cancer screening in the context of both intraorganizational and interorganizational processes. We reviewed 79 studies assessing the relationship between organizational factors and cancer screening. Screening rates are largely driven by strategies to 1) limit the number of interfaces across organizational boundaries; 2) recruit patients, promote referrals, and facilitate appointment scheduling; and 3) promote continuous patient care. Optimal screening rates can be achieved when health-care organizations tailor strategies to the steps and interfaces in the cancer screening process that are most critical for their organizations, the providers who work within them, and the patients they serve. J Natl Cancer Inst Monogr 2010;40:38 57 Cancer screening is effective at reducing morbidity and mortality from breast, cervical, and colorectal cancers (1 4). Screening is a process of care (5), consisting of several steps and interfaces between patients, providers, and health-care organizations. Interruptions, or breakdowns, in the screening process can lead to failure to detect and diagnose cancer promptly (6,7). Approximately half of women aged 50 and older who are diagnosed with late-stage breast cancer have not received a screening mammogram (8), and approximately half of cervical cancers are diagnosed among women who have not been screened in the past 3 years or ever (9). Nonadherence to recommended periodic screening is also an important attributable factor in colorectal cancer mortality, particularly among lower socioeconomic populations (10). Steps and interfaces in the cancer screening process range from patient recruitment to results reporting (Figure 1) and may vary by screening modality (ie, fecal occult blood test [FOBT] vs colonoscopy) and from organization to organization. Screening processes may be divided into two primary categories, represented by the upper and lower branches of Figure 1. The upper branch illustrates screening offered within an organization at the time of a health-care visit, whereas the lower branch illustrates screening offered by referral to another health-care provider or organization. The former category requires intraorganizational coordination of screening activities, whereas the latter requires interorganizational coordination across departmental or organizational boundaries, necessarily resulting in more interfaces and increasing challenges to communication and coordination. Papanicolaou testing for cervical cancer is most often performed as part of an intraorganizational process; mammography, sigmoidoscopy, and colonoscopy are more likely to occur in interorganizational processes, as most primary care practices do not have the facilities, equipment, or trained professionals to perform them (11). FOBTs, which have faded in popularity over the last decade (12), can be self-administered by patients, thereby escaping intraorganizational or interorganizational processes. However, communication and coordination still are required between providers and patients, and between patients and the organizations to which they must return completed tests. Organizational changes have been shown to have a major impact on rates of breast, cervical, and colorectal cancers screening (13). Few studies explore the role of organizational factors in addressing the interfaces presented by intra- and interorganizational screening processes, however. This article reviews what is known about the association between organizational factors and cancer screening rates and examines how organizational strategies can address the steps and interfaces of cancer screening in the context of both intraorganizational and interorganizational processes. Methods Definitions Steps in the cancer screening process are medical encounters or actions, including patient recruitment, attendance at a health-care visit, and performance of a screening test (14) (Figure 1). Interfaces are transfers of information and/or responsibility between patients, providers, and health-care organizations, including provider recommendation or referral to screening, appointment scheduling, and results reporting. Interfaces are not only within and between organizations but also between organizations and providers, organizations and patients, and patients and providers. We use the term health-care organization to refer to entities that provide, coordinate, or refer patients to cancer screening. This definition includes primary care practices, community health clinics, hospitals, and health maintenance organizations, for example, but excludes faith-based organizations or community groups involved in cancer screening promotion or population-level registries used to identify patients in need of screening. 38 Journal of the National Cancer Institute Monographs, No. 40, 2010

2 Figure 1. Steps and interfaces in the cancer screening process. Organizational factors affecting both intraorganizational and interorganizational cancer screening include structures, such as capital or human resources and administrative or fiscal arrangements (15), and processes, activities done to and for patients within these structures (16). Organizational structures and processes can be designed to overcome interface challenges between and among health-care organizations, providers, and patients. We classify organizational factors according to 1) which steps and interfaces they address within the screening process; 2) their target audience (patients and/or health-care providers); and 3) the mechanism through which they change screening behaviors (predisposing, enabling, or reinforcing, per the Precede/Proceed model) (Figure 2) (17). This classification acknowledges that screening is the result of interactions between provider and patient behaviors that occur within organizational contexts. Predisposing factors, such as knowledge, attitudes, perceptions, or beliefs, provide rationale or motivation for behavior. Strategies aimed at positively predisposing patients include counseling or educational materials. Strategies aimed at positively predisposing providers may involve continuing education regarding current evidence-based guidelines, for example. Enabling factors, such as skills, resources, and technology, facilitate patient or provider behaviors. Organizational strategies that enable providers include clinical information systems, such as reminders and delivery system design, including care coordination and management via clinician teams. For patients, enabling strategies include logistical assistance, such as access to convenient transportation and appointment scheduling. Reinforcing factors provide a continuing encouragement, reward, or incentive for behaviors. For example, pay-for-performance initiatives that provide financial rewards for meeting screening targets act as reinforcement for providers. Strategies aimed at reinforcing repeat screening among patients who have screened in the recent past include anniversary reminder mailings, for example. Literature Search We conducted a selective search to identify studies that assessed the association between organizational structures and processes and cancer screening rates. To identify rigorous evaluations of interventions to promote cancer screening occurring within health-care organizations, we gathered references from systematic reviews of interventions to promote screening published in 2008 (18 20) and updated in 2009 (21). Journal of the National Cancer Institute Monographs, No. 40,

3 Figure 2. Classification of organizational interventions by cancer screening steps or interfaces, target audience, and mechanism. Fifty-nine of the referenced articles described interventions occurring within health-care organizations from 1990 through 2008 and were retained for review. To describe the relationship between organizational structure and process factors and cancer screening outside of the intervention context, we searched the MEDLINE database for Englishlanguage articles published from 1990 through 2008, applying the search terms cancer screening and organization or cancer screening and primary care to the title and abstract fields. To locate articles not detected by the search terms, we electronically searched by author for articles by researchers whose previous published work explored organizational influences in cancer screening. We identified articles that may have been missed in electronic searches by manually reviewing references from bibliographies of articles from the initial search and from reviews of cancer screening interventions. These search techniques resulted in 20 nonintervention articles that assessed the relationship between organizational factors and cancer screening. Two of the authors (R. Anhang Price and H. Edwards) reviewed the primary articles, summarized the findings concerning screening outcomes, and identified the target audience (patient or provider), intervention mechanism (predisposing, enabling, or reinforcing), and cancer screening process or interface addressed (recruitment, visit with on-site screening, recommendation and/or referral, appointment scheduling, test performance, or results reporting). Discrepancies were resolved by discussion with all authors. Results Of the 79 studies under review, 49 measured the association between organizational factors and breast cancer screening, 21 measured associations with cervical cancer screening, and 20 measured associations with colorectal cancer screening. Study settings varied considerably and included primary care practices, community health centers, local and national health plans, health maintenance organizations, and Department of Veterans Affairs medical centers. Patient populations included those who had never participated in screening, those who were up to date for screening, and patients with and without health insurance that provided coverage for screening tests. Study details are described in Appendix 1, Tables 1 and 2. Organizational Processes Evidence of the association between organizational processes and cancer screening outcomes is summarized in Table 1. Fifty of the studies we reviewed evaluated the effects of processes to promote patient recruitment; three evaluated visits with on-site screening; 23 provider recommendations or referrals to screening; 15 appointment scheduling; two provider or patient training to perform screening tests; and none reporting of screening test results. Two cross-cutting processes had the potential to influence multiple steps or interfaces by promoting continuity of patient care. Recruitment. Standard reminder mailings effectively increased mammography and Papanicolaou test rates in several settings, including community health centers serving low-income women, health maintenance organizations, and general practices (23,26,46, 47,50,53,58,64,66,70,77), but several other studies conducted in similar settings found standard letters to be no more effective than no letter (28 30,45,65,71). By providing a cue to action, standardized mailings act as predisposing interventions for patients who are up to date for screening or those who have intention to attend timely screening in the future. More intensive predisposing interventions, such as tailored communications, may be needed for patients who are not highly motivated to participate in screening. Tailored mailings or telephone counseling are customized according to patients logistical, cognitive, and affective barriers to screening; intention to participate in screening; past screening behaviors; and/or data available from medical records. There is mixed evidence for the effects of tailored mailings on screening rates; however, tailored telephone counseling has shown more consistently positive results for promotion of mammography. Distribution of FOBT request cards, FOBT kits, and FOBT kits with prepaid postage successfully increased rates of FOBT use in all interventions under study (38,42,49,57,58,62,63); these interventions enable screening by offering patients the tools to perform screening independently, thereby avoiding steps and interfaces of either intra- or interorganizational cancer screening. Visit With On-site Screening. Availability of on-site screening facilities and personnel can reduce the number of interfaces required 40 Journal of the National Cancer Institute Monographs, No. 40, 2010

4 Table 1. Evidence of association between organizational processes and breast, cervical, and colorectal cancer screening outcomes, by cancer screening step/interface, target audience, and behavioral mechanism* Cancer screening step or interface addressed Target audience Breast cancer screening Cervical cancer screening Colorectal cancer screening Behavioral mechanism Behavioral mechanism Behavioral mechanism Predisposing Enabling Reinforcing Predisposing Enabling Reinforcing Predisposing Enabling Reinforcing Recruitment Patient Reminder letter (untailored) (23,46,47,50,53, 58,66,70,77), (29,45,65,71) Tailored mailing (31,47,65,75), (45,54,56,67, 68,72,78) Tailored telephone counseling (31,33,50,55, 56,60,68,70, 74,75,77), (67,78) Tailored computer tutorial (32) Video (32) In-office educational materials (43) In-office counseling (75) Group education (35) Visit with on-site screening Recommendation and/or referral Patient minirecord (36) Patient Same-day mammography (37) Free, on-site mammography (53,80) Provider Physician education (33) Chart reminder (40,52,66,73), (23,29,83) Flow sheet (83) Patient minirecord (36) Nurse completion of referral forms (43) Reminder letter (untailored) (24,27,65) Tailored mailing (31,65), (56,67,72) Tailored telephone counseling (31,33,56), (67) Audit and feedback (39,48), (44) Financial incentives (40,44,69,92, 99) Reminder letter (untailored) (26,47,64,77), (28,30,45) Tailored mailing (45,47,67), (54) Telephone call (26) Tailored telephone counseling (67,77) In-office video (79) Patient minirecord (36) Chart reminder (26,64,73), (30) Patient minirecord (36) Tailored mailing (67) Tailored telephone counseling (67) Audit and feedback (39,48), (44) Financial incentives (69,99), (44) Reminder letter (untailored) (49,61,76) FOBT kit request card (42,62) Reminder call (61,76) Directive prioritizing screening (25) FOBT kit (49,57,62,63) FOBT kits with postage-paid return (38,58) Patient minirecord (36) Chart reminder (76,88) Patient minirecord (36) Patient Referral tear sheet (41) Audit and feedback (48),(44) Financial incentives (22),(44) (Table continues) Journal of the National Cancer Institute Monographs, No. 40,

5 Table 1 (continued). Breast cancer screening Cervical cancer screening Colorectal cancer screening Behavioral mechanism Behavioral mechanism Behavioral mechanism Predisposing Enabling Reinforcing Predisposing Enabling Reinforcing Predisposing Enabling Reinforcing Target audience Cancer screening step or interface addressed Letter with appointment time (64) Letter with direct access to appointment (no referral) (73) Scheduling telephone call (54) Patient Letter with appointment time (46) Letter with direct access to appointment (no referral) (52,73), (71) Scheduling telephone call (24,27,34, 54,58,60,74,77) Appointment scheduling Test performance Provider Physician education (33) Patient Instructional telephone call (61) * Bolded citations indicate a significant association between the organizational variable and cancer screening. Italicized citations indicate no association. In some cases, associations are negative. Jibaja-Weiss, Volk, Kingery, Smith and Holcomb (47) found a negative association between tailored letters and Papanicolaou test and mammography participation; Wee, Phillips, Burstin, et al. (99) found a negative association between provider productivity incentives and Papanicolaou test provision. FOBT = fecal occult blood test to complete screening and enable patient participation by helping to overcome time-, cost-, and transportation-related barriers. Patients offered the opportunity to receive a mammogram nearby immediately after scheduled internal medicine appointments were significantly more likely to receive mammograms than those who were required to schedule a mammogram for a later date (37). Provision of free on-site screening at community health centers either in a bimonthly mammography van or a routinely available traditional mammography facility was also associated with increased screening participation among low-income women (53,80). Recommendation and/or Referral. Provider recommendation is strongly associated with patient screening behavior (101). Chart reminders, either electronic or paper prompts that remind clinicians that a patient is due for screening, were assessed by 10 studies under review. Positive associations were found for four of seven reminders of mammography (40,52,66,73), three of four reminders of Papanicolaou testing (26,64,73), and two of two reminders of colorectal cancer screening (76,88). Chart reminders have a more limited reach than recruitment strategies, as they enable screening only among those patients who attend a health-care visit or those who attend visits but fail to receive screening. Audit and feedback interventions consist of medical chart reviews for patients screening eligibility, referral and completion, and verbal or written feedback to clinicians regarding their compliance with screening guidelines. These interventions reinforce providers screening behaviors by underscoring the importance of screening and stimulating changes in screening practices, as needed. Two primary studies of audit and feedback among medical residents reported increases in referral to mammography or sigmoidoscopy and completion of Papanicolaou testing and/or FOBT (39,48). A third study of primary care physicians found no association between feedback and on-site screening for cervical cancer or referral to off-site breast or colorectal cancer screening (44). Productivity and quality incentive payments, sometimes referred to as pay for performance, have been proposed to reinforce clinician behaviors. However, little empirical evidence supports their effectiveness (102). In our review, the six studies evaluating financial incentives reported mixed results. Token rewards of less than $100 were not associated with increases in mammography referral among primary care physicians (40); similarly, small periodic bonuses offered to primary care practice sites based on compliance with breast, cervical, and colorectal cancers screening were ineffective (44), as were quarterly bonuses to multispecialty physician organizations (69). The latter study did find a positive association between bonuses and Papanicolaou test administration, however. Armour et al. (22) found that an end-of-year bonus for primary care physicians treating managed care patients was associated with increased referral to colorectal cancer screening, especially FOBT. Wee, Phillips, Burstin, et al. (99) found that patients of physicians paid by salary plus productivity incentives were significantly less likely to receive Papanicolaou tests than patients of physicians paid by salary only. Together, the findings of these studies suggest that financial incentives may be more influential when targeted to individual clinicians, rather than to physician groups, when they are large enough to be meaningful and noticeable to their recipients, and when the targeted behaviors do not require further interfaces of 42 Journal of the National Cancer Institute Monographs, No. 40, 2010

6 Table 2. Evidence of association between selected organizational structures and breast, cervical, and colorectal cancer screening outcomes* Organizational structures Breast cancer screening Cervical cancer screening Colorectal cancer screening Practice size Patient volume (92,97) (97), (92) (97,100) Number of providers (94,85), (95) (94), (85) (95) Practice type Academic vs community-based private practices vs health maintenance (98) organizations Integrated medical group vs independent practice association (92) (92) Multispecialty vs single specialty practice (86) Resources or facilities for screening (97) (97) (81,97,100), (86) Nonphysician personnel to identify screening-eligible patients (83) Staffing mix (ratio of generalists to specialists) (97) (97) (97,100) Organizational culture (perceived commitment to service quality) (85) (85) * Bolded citations indicate a significant association between the organizational variable and cancer screening. Italicized citations indicate no association. In some cases, associations are negative. Soban and Yano (97) and Yano, Soban, Parkerton and Etzioni (100) found that higher patient volume is a negative predictor of cancer screening tests; Greiner, Engelman, Hall, and Ellerbeck (86) found that having no endoscopy available in the practice was significantly associated with patients self-report that they were up to date on colorectal cancer screening. care (ie, appointment scheduling and/or administration of screening tests by an additional health-care provider at a later time, as in the cases of mammography or colonoscopy). Financial incentives, like all organizational strategies that enable or reinforce provider referral, may be more effective in achieving increased screening participation when screening is provided in an intraorganizational process, rather than an interorganizational one. Appointment Scheduling. Enabling appointment scheduling through telephone calls was associated with increases in mammography use in all eight studies that assessed this approach (24,27,34,54,58,60,74,77); an additional study found a positive relationship between scheduling telephone calls and use of Papanicolaou tests (54). Some of these telephone call interventions combined scheduling and tailored counseling; however, the scheduling component, rather than counseling, was likely the primary mechanism for improved patient screening in many instances [see, eg (34,74)]. Test Performance. Training can predispose or enable clinicians to recommend or conduct screening. Training or education that transmits screening data or recommendations may build the knowledge base that predisposes a clinician to recommend screening, whereas skills-based courses may enable providers to perform new or unfamiliar screening tests. Similarly, instruction can enable patients to perform self-tests like FOBT, when available. In our review, an educational curriculum for physicians emphasizing instruction in mammography counseling and clinical breast examination did not significantly alter patients mammography adherence, as most of the physicians under study participated in only part of the program (33). However, an instructional telephone call to patients regarding how to use FOBT kits was successful in promoting FOBT use (61). Results Reporting. No studies under review focused explicitly on enabling reporting of screening test results. Cross-cutting Organizational Processes. In addition to organizational processes designed to address specific steps and interfaces in cancer screening, our review identified processes aimed at improving continuity of care. Joint responsibility for patients across clinicians in a group practice especially among those who have worked together over an extended tenure was shown to facilitate improvements in breast and cervical cancer screening rates (94). Patient assignment to primary care providers in Department of Veterans Affairs medical centers was associated with improvements in breast cancer screening rates, but not cervical cancer screening rates (85). Organizational Structures Evidence of the association between selected organizational structures and cancer screening outcomes is summarized in Table 2. Like the cross-cutting organizational processes mentioned above, organizational structures have the potential to influence multiple steps and interfaces in cancer screening. A positive relationship between patient volume and clinical outcomes has been established for many procedures, including cancer surgeries (103,104), but provision of preventive care services may suffer in a high-volume practice environment (105). Our review found mixed evidence for the relationship between patient volume and cancer screening adherence. Studies of Department of Veterans Affairs medical centers and primary care practices found that higher patient volume was a strong negative predictor of breast, cervical, colorectal cancers screening (97,100), whereas a study of California physician groups found no relationship between patient volume and rates of cervical screening, and a positive relationship between volume and mammography rates (92). There are also conflicting findings for the association between the number of providers in a provider group another measure of practice size and screening rates. One study reported that physicians in group practice were no more or less likely to provide mammograms or colon cancer screening to Medicare beneficiaries than physicians in solo practice (95), whereas another study attributed higher rates of up-to-date colorectal screening in group or multispecialty practices to time to discuss screening, rather than to the screening capacity of group practices (86). The effects of organizational size and practice type may be mediated by the presence of care processes to promote screening, efforts to coordinate across health-care providers and organizational units, and the human and capital resources dedicated to screening. Journal of the National Cancer Institute Monographs, No. 40,

7 Availability of facilities and staff for screening has the potential to increase the likelihood that patients receive screening on-site. Our review found mixed results regarding this relationship. Studies of Department of Veterans Affairs medical centers and primary care practices reported that sufficiency of appropriately equipped examining and treatment rooms, equipment for pelvic exams, personal computers, and patient education space was associated with higher rates of cervical and colorectal cancer screening (97,100). A positive association was not found for breast cancer screening, however, perhaps because the screening resources assessed did not include mammography equipment (97). Availability of flexible sigmoidoscopy in family practices was shown by one study to be positively associated with increased likelihood of patients having up-to-date colorectal screening (81). A study of rural primary care practices did not find an association between availability of endoscopy in the practice and increased rates of screening (86), and attributed failure to screen to inadequate discussions between clinicians and patients. These findings suggest that facilities and equipment for screening can influence screening by allowing for intraorganizational screening, but that resources alone may be in - sufficient in the absence of efforts to promote patient recruitment, provider recommendation, and patient provider communication. Nonphysician personnel to identify patients eligible for screening mammography was not found to be significantly associated with mammography rates in one study of primary care practices (83). Although administration of screening by nonphysician staff has been suggested to expand capacity, especially in the context of colorectal cancer screening (106), no studies in our review assessed the effects of assigning nonphysician personnel to perform screening. Discussion Given sparse data and mixed findings, we cannot make conclusive statements about the relationship between specific organizational factors and cancer screening outcomes. Nonetheless, we can infer a theme: Organizational structures, such as practice size and type, do not dictate screening rates for a given organization. Rather, screening rates are largely driven by strategies to 1) limit the number of interfaces across organizational boundaries; 2) recruit patients, promote referrals, and facilitate appointment scheduling; and 3) promote continuous patient care. Limiting Interfaces Through On-site Screening. Interorganizational screening processes, which require interfaces across departmental and organizational boundaries, are often challenged by incompatibility of information technology systems, loss of information during patient handoff, and limited financial reward for successful interorganizational transfers of information and responsibility. Whenever possible, strategies to promote on-site screening reduce the number of interfaces for organizations, health-care providers, and patients, and thereby increase the likelihood that patients are screened. For this reason, on-site, same-day screening mammography was among the most consistently effective organizational strategies in our review. Addressing Steps and Interfaces. A number of organizational strategies can influence steps and interfaces in both intra- and interorganizational screening processes. Stepped approaches to recruitment, beginning with inexpensive, standardized reminder letters for patients who are highly motivated to screen, and advancing, as needed, to tailored mailings or telephone counseling to predispose and reinforce patient screening, are well supported by the literature, and address the first interface in Figure 1. Such outreach reminders do not necessitate a provider patient encounter. For patients who attend health-care visits, reminders to clinicians enable inreach, improved recommendation or referral to screening, as well. Strategies to reinforce provider screening referrals and recommendation, such as financial incentives, have been less effective than enabling interventions, such as chart reminders. Providing Continuous Care. Ensuring that patients pass through each of the necessary steps and interfaces requires strategies that address not only each step and interface individually but also emphasize continuous flow across the screening process. Studies in our review reported conflicting results for the relation between usual provider continuity, care of a patient by a single health-care provider or provider team over time, and breast and cervical cancer screening (84,89,93,94). Mixed findings are not surprising because continuity is not an inherent organizational feature, but rather the product of organizational structures and processes designed to ensure that patients do not get lost in interfaces with health-care providers and organizations. Continuity can be classified into three categories: 1) informational continuity, the use of information about patients histories and personal circumstances to make care decisions; 2) management continuity, the delivery of appropriate and timely health-care services that respond to patients changing needs; and 3) relational continuity, an ongoing therapeutic relationship between patients and their provider(s) (107). All three types of continuity may influence interface activities by affecting whether providers know a patient s screening status, whether a patient is seen regularly and receives routine screening reminders, and whether a patient has an ongoing relationship with a health-care provider whose recommendations he or she trusts. A number of proven organizational strategies can address the types of continuity. For example, informational continuity can be fostered through consistent use of electronic medical records, management continuity through development and implementation of practice guidelines and protocols, and relational continuity through role assignments that free clinicians to see patients for longer visits (108). Applying Research Findings in Practice Identifying Organizational Priorities for Improving Screening Rates. Cancer screening may be promoted or impeded by factors at several levels, including characteristics of the patient; characteristics of the health-care provider and of the health-care team in which the provider works; the organization or practice setting in which the screening test takes place; and the larger health-care environment (14). Consequently, the success of organizational strategies to promote screening depends on characteristics of the organization, the providers who work within it, and the patients it serves. For example, predisposing strategies may be necessary for some providers and patients, but insufficient in the absence of enabling and reinforcing strategies. To select and prioritize strategies, organizations must assess their performance at each step and interface of the 44 Journal of the National Cancer Institute Monographs, No. 40, 2010

8 cancer screening process, and examine the causes of process breakdowns at the organizational-, provider-, and patient-level. Successful organizational strategies will vary by screening modality and for each organization, and must reflect interfaces across departments or organizational boundaries. Adapting Organizational Processes and Interventions for Implementation. Once priority screening steps and interfaces are identified, proven strategies must be tailored to the particular organization. Tailoring involves retention of the strategy s core components, such as counseling or appointment scheduling, and adaptation of peripheral elements, such as counseling messages or timing of appointments, to integrate the strategy into the organization s ongoing activities (109). Tailoring strategies based on assessments of practices clinical operations, culture, approaches to prevention, and relationships between personnel have been shown to increase cancer screening in primary care practice settings (110) and may be particularly useful for improving intraorganizational screening processes. Implementation of screening process improvements is influenced by factors both internal and external to the organization. These factors have been codified in a model of primary care practice change that considers interrelationships between motivation of key stakeholders, such as medical directors or others who influence the behavior of the clinical practice; resources for change, such as management infrastructure, communication, and leadership; outside motivators, such as events and systems in the community and health-care environment; and perceived opportunities to make changes (111). Stakeholder motivation stems from a belief in the importance and effectiveness of systems approaches to improve screening; however, many practice leaders and clinicians do not hold this belief (51). Consistent and committed leadership is required to help organizations overcome the resistance and disruptions that may result from process changes (112). Priorities for Future Research Our review identified more than 40 discrete organizational factors that may promote cancer screening, encompassing most of the commonly measured factors of health-care organizations (113). However, some important organizational features are notably absent in the cancer screening studies we reviewed. For example, both team effectiveness and quality reporting have been associated with organizational changes and processes that improve care quality, especially for chronic conditions [see, eg, (114,115)]. The ways in which organizations address competing demands of acute, chronic, and preventive care also substantially affect the likelihood that patients receive adequate preventive services (116). Organizational leaders commitment is also critical to pursuit of quality improvements (117). These concepts are worthy of further assessment in the context of cancer screening, as the comprehensive set of organizational factors shown to influence chronic and acute care may be relevant in the context of preventive care, as well (118). Few of the studies in our review examined the component steps and interfaces within organizations cancer screening processes or explicitly described the interdepartmental or interorganizational communication and coordination that needed to occur to accomplish cancer screening. Assessment of the intra- or interorganizational cancer screening process is a critical first phase for the development and implementation of effective organizational solutions and is a priority for future research. Development and application of measures that systematically describe organizational factors that influence screening steps and interfaces for both intraand interorganizational processes would result in actionable findings for health-care organizations seeking to improve screening. Ideally, organizational strategies to improve screening should address ongoing cancer screening performance that is, screening participation leading to appropriate follow-up among those with abnormal results and repeated routine screening among those with normal results (119). However, the vast majority of studies in our review measured single screening events. Future research should address the effectiveness of organizational factors to promote long-term screening that bridges the transition to diagnosis and treatment, as needed. Limitations Our review has a number of important limitations. First, the search terms and techniques we applied may have missed some relevant articles. In particular, we included only those intervention studies that met the rigorous inclusion criteria of the Task Force on Community Preventive Services (120). Second, we focused on organizational structures and processes associated with cancer screening. Much research has investigated the association between organizational factors and a variety of other health-care outcomes, most notably patient safety and chronic care delivery. A number of systematic measurement tools, including the Assessment of Chronic Illness Care, the Survey of Organizational Attributes for Primary Care, and clinical microsystem assessments, are available to evaluate organizational attributes and assess strengths and weaknesses in care delivery ( ). This extensive body of work is beyond the scope of our review. Integration of cancer screening as a prevention outcome in this work is a critical priority, as is the development of systematic organizational approaches that span across different types of preventive care services (124). Third, much of the intervention literature we reviewed focused on improving mammography and FOBT participation; further research is needed on organizational factors to improve cervical and colorectal cancer screening, as the cancer screening process and the organizational factors that influence it varies by screening modality. Finally, as new screening tests emerge, existing tests grow in popularity, and clinical guidelines are updated, the cancer screening process must be reexamined to determine which steps and interfaces are most critical. Conclusions A variety of organizational strategies has the potential to improve cancer screening rates substantially by limiting the number of interfaces across organizational boundaries; recruiting patients, promoting referrals, and facilitating appointment scheduling; and promoting continuous patient care. Optimal screening can be achieved if health-care organizations tailor their organizational processes to the cancer screening steps and interfaces that are most critical for their organizations, the providers who work within them, and the patients they serve. Journal of the National Cancer Institute Monographs, No. 40,

9 Appendix 1: Organizational Factors and the Cancer Screening Process Appendix Table 1. Description of organizational intervention studies* Reference Patient population Provider population or practice setting Intervention Armour et al. (22) Commercially insured patients aged 50 and older in a managed health-care plan Bankhead et al. (23) Women who had failed to attend a recent appointment for routine third-round breast screening Barr et al. (24) Women aged who had had a previous mammogram, but not one within the previous 18 months Primary care physicians End-of-year bonus designed to increase colorectal cancer screening; bonus not described. General practices not meeting a target of 70% mammography coverage, United Kingdom Group model HMO, with most members privately insured Letters from physicians encouraging women to reconsider their decisions not to attend breast screening. Prompt in paper medical records for physicians to discuss breast screening at any routine consultation. Mail reminder indicating a mammogram was due and offering encouragement for the patient to call and schedule an appointment. Telephone call from medical center staff person containing the same information provided in the mailing and giving opportunity to schedule an appointment for clinical breast exam and mammogram referral. Battat et al. (25) VA patients Physicians practicing at VA hospitals Colorectal cancer screening chosen as a performance measure in a quality improvement initiative. Screening directive was issued and implemented (no further details given). Binstock et al. (26) Women aged who had not had a Papanicolaou test in the past 3 years Bodiya et al. (27) Women aged 50 and older who had had a mammogram in the previous year and were due for the next annual screening Buehler and Parsons (28) Women aged who had not had a Papanicolaou test in the previous 3 years Burack et al. (29) Urban minority women aged 39.5 and older who had attended a visit in the previous 18 months Burack et al. (30) Women aged who had attended a visit in the previous year Champion et al. (31) Women aged 51 and older with no mammogram in the previous 15 months HMO patients were primarily white, whereas clinic patients were primarily African American Champion et al. (32) African American women aged who had not had a mammogram within the last 18 months and were at or below 175% of the poverty level Costanza et al. (33) Women aged who never had a mammogram, had a mammogram but not in the previous 24 months), or had received a mammogram in previous 24 months, but none in the 24 months before that HMO with outpatient medical centers Telephone call and letter to patients. Patient chart reminder and memo to primary care provider. Family practice Reminder letter to women. The letter plus telephone calls by medical assistants, who arranged mammograms and processed referral forms. Family medicine clinics in Newfoundland, Canada Letters on the Provincial Cytology Registry s letterhead. HMO Reminder letter mailed to patients was personalized and signed by the medical director of the HMO. Physician reminder notice placed at the front of patient s medical chart. HMO Reminder letter mailed to patients was personalized and signed HMO General medicine clinic serving low-income clients General medicine clinic serving low-income clients Participants also recruited from multiservice center and an African American convention HMO Primary care providers by the medical director of the HMO. Physician reminder was a notice placed at the front of patient s medical chart. Tailored mailing personalized using woman s name, her primary care provider s signature, and tailored information regarding her perceived risk, benefits, and barriers to mammography. Tailored telephone counseling was similar in content to the mailing. Combination of tailored mailing and tailored phone counseling. Tailored interactive computer program tutorial included questions and tailored messages in response to participants knowledge of, beliefs about, and barriers to, cancer screening. Targeted videotape, using same video clips as computer program. Barrier-specific telephone counseling identified and addressed specific barriers to mammography. Physician education course including skills practice and role-play and including a $150 incentive to participate. Course follow-up included videos, manual on office systems development, and a free workshop for office staff to improve tracking and follow-up of patient mammography participation. (Table continues) 46 Journal of the National Cancer Institute Monographs, No. 40, 2010

10 Appendix Table 1 (continued). Reference Patient population Provider population or practice setting Intervention Davis et al. (34) Women aged who had not had a mammogram in the previous 18 months Davis et al. (35) Predominantly low-income, African American women aged 40 and older who had not had a mammogram in the previous 12 months Dickey et al. (36) English- and Spanish-speaking patients aged who had visited the provider in the previous 14 months and returned to the provider within 18 months Dolan et al. (37) Women aged 50 and older who had not had a mammogram in the past 12 months Freedman and Mitchell (38) Predominantly uninsured and Medicaid-covered patients, approximately two-thirds black Goebel (39) Internal medicine patients, 75% of whom are covered by Medicare or private insurance Grady et al. (40) Female patients aged 50 and older, attending primary care practices Harris et al. (41) Patients aged 50 and older who had a first-degree relative with a history of colorectal cancer HMO Telephone call to patients to schedule an appointment for mammography or address patients explanations for refusing to schedule a mammogram. Mammography letters were mailed to those who refused to schedule. Outpatient clinics Personal recommendation to get a mammogram; personal recommendation plus brochure; or one-time group education program, including a soap-opera video. Inner-city family health clinic The patient-held minirecord, or Health Diary, in English or Urban academic general internal medicine practice with a nearby hospital mammography center Spanish, described nature and timing of preventive services and had a chart for recording dates and results of preventive services. Nursing staff distributed information sheets to patients and clipped the Health Diary to the medical record. The provider gave the diary to the patient, explained its use, and filled out the record. Opportunity to receive a mammogram at a facility three blocks away immediately after scheduled internal medicine appointment. Free bus transportation to the screening facility. Inner-city clinic Return completed FOBT cards in person, in addressed envelopes without postage, or in addressed, postage-paid envelopes. Medical residents Peer review feedback program, in which physicians reviewed colleagues charts and returned them. Original physician completed a form explaining lack of compliance or making a plan for the future. Attending physician reviewed for accuracy and offered feedback. Primary care physicians Cue enhancement of posters in waiting and treatment rooms and chart stickers for women aged 50 and older that have spaces for recording three mammogram referrals or completions. Cues plus feedback rewards, individualized feedback consisting of a chart illustrating the physician s percent of referrals and patient completions compared with the averages for all physicians in the study, and another chart comparing mammography compliance rates for each physician s patients with the average rate for all physicians in the study. Token rewards consisted of a check based on the percent referred during each audit period. General practices in Australia Pamphlet with information about risk, screening tests, and a tear-off page requesting FOBT. Hart et al. (42) Patients aged Large group practice in Britain Invitations to receive free FOBT tests were mailed. Some patients received a leaflet about colorectal cancer screening in addition to the invitation. Herman et al. (43) Women aged 65 and older Public hospital Patient educational materials, including a mammography pamphlet and a sheet outlining the importance of mammography for older women, were given to patients by the nurse at each clinic visit. The nursing staff could complete the radiology request form for screening mammography and attach it to the patient s chart. (Table continues) A health maintenance flow sheet was attached to each patient s chart, and this was updated at each visit. Journal of the National Cancer Institute Monographs, No. 40,

11 Appendix Table 1 (continued). Reference Patient population Provider population or practice setting Intervention Hillman et al. (44) Female patients aged 50 and older, covered by Medicaid-managed care, 76% black Hogg et al. (45) Patients who had visited the office at least once in the previous 24 months Primary care physicians treating Medicaid-managed care patients Semiannual feedback to primary care providers regarding compliance with screening guidelines: reports documented a site s scores on each screening measure, a total score across all screening types, and plan-wide scores for comparison. Three intervention sites with highest compliance scores received a bonus of 20% of capitation for all female members aged 50 and older, the next three sites received 10% bonuses. Family medicine center in Canada Form letter reminder to families. Customized letter to families, including one page for each family member outlining each preventive procedure for which the patient is eligible, as determined by age, sex, family history, and previous illness. Irwig et al. (46) Women aged General practices in Australia Patient reminder letters with and without stated appointment times. Jibaja-Weiss et al. (47) Predominantly minority, low-income women, aged Community health centers Some patients were mailed a form letter that contained generic information. Other patients received tailored letter content modified to address specific risk factor data from women s medical charts, including age, race/ethnicity, family history, parity, body mass index, and smoking status. Kern et al. (48) Primary care patients Medical residents Four or more charts we are audited per year by a committee of attending physicians. Residents received a detailed typewritten summary of the findings, comments from the reviewers, an analysis of strengths and weakness in performance, and suggestions for future improvement. King et al. (49) Australian general public aged 45 and older Community intervention with support of General practitioner letter, with or without description of dietary general practices in Australia restrictions, FOBT kit, and colon cancer brochure. King et al. (50) Women aged HMO Reminder letter sent 45 days after breast cancer information Kinsinger et al. (51) Patients of family medicine and general internal medicine practices Landis et al. (52) Women aged who had been seen twice or more in the previous 24 months and had not had a mammogram in the previous 12 months Family and internist physicians, primarily fee-for-service, half group practices, half solo practitioners packet with free mammogram referral was mailed to women. Second reminder letter and preventive office visit letter urging women to have a checkup, or telephone counseling. Counseling content was guided by scripted responses to 26 possible barriers to screening. Practices were encouraged to implement office systems and practice policies, including tools for tracking and prompting screenings and patient education materials. Family health center Physician prompts were computer-generated cards attached to patient s charts indicating that the patient was eligible for screening mammography and had not had a mammogram in the previous year. The patient letter encouraged all female patients aged to have annual screening mammograms, indicated that the records showed that the patient was not up to date with screening, and included a prescription for patients to call and schedule a mammogram directly. Lane and Burg (53) Underserved female patients aged 50 and older Community health centers Mammography provided at health center sites approximately once per month in a mammography van; charges were waived for those without insurance. (Table continues) 48 Journal of the National Cancer Institute Monographs, No. 40, 2010

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