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Original Investigation |

Patient and Physician Reminders to Promote Colorectal Cancer Screening:  A Randomized Controlled Trial FREE

Thomas D. Sequist, MD, MPH; Alan M. Zaslavsky, PhD; Richard Marshall, MD; Robert H. Fletcher, MD; John Z. Ayanian, MD, MPP
[+] Author Affiliations

Author Affiliations: Division of General Medicine and Primary Care, Brigham and Women's Hospital (Drs Sequist and Ayanian), Department of Health Care Policy, Harvard Medical School (Drs Sequist, Zaslavsky, and Ayanian), Harvard Vanguard Medical Associates (Drs Sequist and Marshall), and Department of Ambulatory Care and Prevention, Harvard Medical School (Dr Fletcher), Boston, Massachusetts.


Arch Intern Med. 2009;169(4):364-371. doi:10.1001/archinternmed.2008.564.
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Published online

Background  Screening reduces colorectal cancer mortality, but effective screening tests remain underused. Systematic reminders to patients and physicians could increase screening rates

Methods  We conducted a randomized controlled trial of patient and physician reminders in 11 ambulatory health care centers. Participants included 21 860 patients aged 50 to 80 years who were overdue for colorectal cancer screening and 110 primary care physicians. Patients were randomly assigned to receive mailings containing an educational pamphlet, fecal occult blood test kit, and instructions for direct scheduling of flexible sigmoidoscopy or colonoscopy. Physicians were randomly assigned to receive electronic reminders during office visits with patients overdue for screening. The primary outcome was receipt of fecal occult blood testing, flexible sigmoidoscopy, or colonoscopy over 15 months, and the secondary outcome was detection of colorectal adenomas.

Results  Screening rates were higher for patients who received mailings compared with those who did not (44.0% vs 38.1%; P < .001). The effect increased with age: +3.7% for ages 50 to 59 years; +7.3% for ages 60 to 69 years; and +10.1% for ages 70 to 80 years (P = .01 for trend). Screening rates were similar among patients of physicians receiving electronic reminders and the control group (41.9% vs 40.2%; P = .47). However, electronic reminders tended to increase screening rates among patients with 3 or more primary care visits (59.5% vs 52.7%; P = .07). Detection of adenomas tended to increase with patient mailings (5.7% vs 5.2%; P = .10) and physician reminders (6.0% vs 4.9%; P = .09).

Conclusions  Mailed reminders to patients are an effective tool to promote colorectal cancer screening, and electronic reminders to physicians may increase screening among adults who have more frequent primary care visits.

Trial Registration  clinicaltrials.gov Identifier: NCT00355004

Figures in this Article

Colorectal cancer is the second leading cause of cancer mortality in the United States.1 Screening programs involving fecal occult blood testing (FOBT), flexible sigmoidoscopy, and colonoscopy lower the incidence of colorectal cancer by removing precancerous adenomas, detect cancers at more curable early stages, and reduce colorectal cancer mortality.26 National guidelines strongly recommend screening for colorectal cancer for average-risk adults 50 years and older.79

Unfortunately, only 60% of eligible adults report up-to-date screening.10 Patients cite lack of motivation and awareness of the need for colorectal cancer screening, and many report that their health care provider did not recommend screening.11 During office visits, physicians may have insufficient time to discuss the growing number of recommended preventive services.12 Physicians report patient requests and reminder systems as 2 main factors that facilitate screening.13,14

Patients may benefit from increased awareness of their need for colorectal cancer screening and encouragement to obtain this service, while physicians may benefit from receiving patient-specific, timely information regarding their patients' screening status. However, except for 2 studies that compared the effects of colorectal cancer screening reminders focused on patients and physicians nearly 20 years ago,15,16 most prior interventions to promote colorectal cancer screening have focused on either patients1722 or physicians.2328 Therefore, we conducted a randomized controlled trial to compare the individual and joint impact of personalized mailings to patients and electronic reminders to primary care physicians to promote colorectal cancer screening within a multisite group practice.

STUDY SETTING

This 15-month trial was conducted from April 2006 to June 2007 at Harvard Vanguard Medical Associates (HVMA), a multispecialty group practice composed of 14 ambulatory health care centers in eastern Massachusetts. Since 1997, clinical practices within HVMA have used a common electronic health record (Epic Systems Corporation, Verona, Wisconsin) that includes clinical notes, diagnostic codes, procedure codes, and laboratory results. The record also supports computerized ordering of all laboratory tests and referrals. Each primary care physician at HVMA practices at a single health care center. Gastroenterologists perform procedures either at an ambulatory endoscopy center operated by HVMA or within an affiliated hospital-based endoscopy center. Manual medical record reviews indicated that electronic documentation of colonoscopies performed at 2 health centers that contract for this procedure with outside gastroenterologists were incomplete, so these 2 centers were excluded. After pilot testing our interventions at one other health care center, 11 health care centers were included in the randomized trial.

PATIENT AND PHYSICIAN ELIGIBILITY

We identified 59 181 patients aged 50 to 80 years who had a visit with 1 of the 110 primary care physicians at 11 centers during the prior 18 months (Figure 1). From this cohort, we excluded 37 321 patients (63%) who had been screened for colorectal cancer in accordance with the HVMA clinical guideline, having received either flexible sigmoidoscopy within 5 years along with FOBT in the prior year or colonoscopy within 10 years. The remaining 21 860 patients (37%) and their 110 primary care physicians were eligible for our study.

Place holder to copy figure label and caption
Figure 1.

CONSORT (Consolidated Standards of Reporting Trials) diagram of patient and physician eligibility and randomization. For the patient mailing, patients were randomized within physician panels, and for the electronic reminders, physicians were randomized within each health center.

Graphic Jump Location

Screening tests were ascertained via an automated electronic algorithm using laboratory results, diagnostic codes, procedure codes, and outpatient and hospital encounters from the electronic record. Compared with physician medical record review for a random sample of patients, this algorithm was 88% sensitive (95% confidence interval [CI], 79%-93%) and 96% specific (95% CI, 87%-100%) in identifying screening tests. Appropriate screening was typically undetected by the automated algorithm when colonoscopy occurred at outside hospitals, particularly before patients received care at HVMA.

The Harvard Medical School and HVMA Human Studies Committees approved the study protocol, including a waiver of informed consent for both patients and physicians because the study was promoting the HVMA standard of care for colorectal cancer screening.

PATIENT INTERVENTION

Patients overdue for colorectal cancer screening received a mailing with the following 4 components: (1) a cover letter from the HVMA chief medical officer identifying the patient as overdue for screening and indicating the dates of their most recent screening examinations, (2) an educational pamphlet detailing screening options, (3) an FOBT kit with 3 Coloscreen stool cards from Helena Laboratories Corporation, Beaumont, Texas, instructions, and a stamped return envelope, and (4) a dedicated telephone number to schedule flexible sigmoidoscopy or colonoscopy. The initial mailing occurred during the first month of the intervention, and a second mailing was sent to patients still overdue for screening 6 months later. When patients called to schedule a colonoscopy, physician assistants screened them for contraindications and provided instructions. Primary care physicians were notified of patients with potential contraindications.

PHYSICIAN INTERVENTION

Throughout the 15-month intervention period, physicians received electronic reminders during office visits with their patients overdue for colorectal cancer screening. Immediately prior to the intervention, we educated physicians in both the intervention and control groups regarding the use of these reminders via a 1-hour presentation and discussion at each center. The alerts were present in both a passive and active form within each patient's electronic medical record. Physicians could view the passive alert at any point during an encounter within the electronic visit summary screen, while the active alert required acknowledgment from physicians attempting to place electronic orders (Figure 2). The alerts provided details regarding the most recent screening tests and facilitated “1-click” electronic ordering of screening examinations. Electronic orders for endoscopic procedures were automatically forwarded to the gastroenterology department for scheduling. Physicians did not receive similar alerts for other preventive services during the intervention period.

Place holder to copy figure label and caption
Figure 2.

Active electronic reminders were delivered to physicians during office encounters and facilitated electronic ordering of recommended tests.

Graphic Jump Location
RANDOMIZATION PROCESS

The patient intervention was randomized at the level of individual patients within each physician's patient panel. Among all 59 181 patients aged 50 to 80 years, we estimated a multivariable logistic regression model for their propensity to have been screened for colorectal cancer at baseline in accordance with the HVMA clinical guideline (Figure 1). Predictors included patient age, sex, race, insurance coverage, and socioeconomic characteristics based on linking patient 5-digit ZIP codes to the 2000 US Census data, including proportion of high school graduates, median household income, and proportion of households below the federal poverty level. Within each physician panel, we paired patients overdue for screening with similar values of this propensity and randomly assigned 1 patient in each pair to receive the intervention mailing, thus closely balancing treatment groups on characteristics related to their baseline screening propensity.

The physician intervention was randomized at the physician level. Within each health care center, we paired physicians with similar colorectal cancer screening rates and numbers of patients overdue for screening and then randomly assigned 1 physician in each pair to receive electronic reminders. We repeated the randomization 20 times and chose the assignment that provided the best overall balance on these 2 characteristics between the intervention and control groups.

STUDY OUTCOMES

All data were collected from the electronic record, and study outcomes were assessed 15 months following the start of the intervention for all randomized patients. The primary study outcome was completion of 1 of the following 3 options during the 15-month study period: FOBT, flexible sigmoidoscopy, or colonoscopy.79 We did not include barium enema examination because it is rarely used for screening purposes at HVMA. Because the detection and removal of precancerous adenomas is a major objective of colorectal cancer screening,29 the secondary study outcome was detection of adenomas based on diagnostic codes. A visual review of electronic records found that these codes had a positive predictive value of 94% (95% CI, 84%-99%) and negative predictive value of 96% (95% CI, 86%-100%) for identifying colorectal adenomas. For a random 10% sample of patients who had colorectal adenomas removed during the study, we conducted medical record reviews to identify the following high-risk findings: (1) 3 or more adenomas, (2) adenoma 10 mm or greater in diameter, or (3) adenoma with villous histologic features. We also ascertained new diagnoses of colorectal cancer via the presence of a new International Classification of Diseases, Ninth Revision, Clinical Modification code of 153.0 to 153.9 or 154.0 to 154.1. We then conducted medical record reviews to verify the diagnosis of colorectal cancer and collect staging data.30

PHYSICIAN SURVEY

We surveyed all 43 of the original 55 physicians in the electronic reminder intervention group who were still practicing at HVMA 4 months after the study ended. The survey instrument assessed perceived effectiveness of colorectal cancer screening modalities and of the electronic reminders using a 3-point Likert scale of “very effective,” “somewhat effective,” or “not effective.” Physicians also identified which screening test they most commonly recommended, as well as the perceived proportion of electronic reminders that accurately reflected patients' screening status. The surveys were administered in a 3-stage process that involved an initial paper mailing, followed by a reminder e-mail and a final paper mailing.

DATA ANALYSIS

All analyses were conducted on an intention-to-treat basis. Baseline characteristics for patients in the intervention and control groups were compared using the Pearson χ2 test for dichotomous variables and an unpaired t test for continuous variables. We analyzed the impact of the interventions by fitting a single linear regression model to predict performance of an appropriate screening examination after adjusting standard errors for clustering of patients by physician. Independent variables included patient intervention status, physician intervention status, and physician baseline screening rate, and we also tested the interaction of patient and physician intervention status.

We fit separate models for prespecified subgroup analyses according to characteristics known to affect rates of colorectal cancer screening, including age (50-59, 60-69, or 70-80 years), sex, and number of primary care visits (0, 1-2, or ≥3).3133 All analyses were performed using SAS version 9.1 statistical software (SAS Institute Inc, Cary, North Carolina), and we report 2-tailed P values or 95% CIs for all comparisons.

STUDY SUBJECTS

We studied 110 primary care physicians and their 21 860 patients who were overdue for colorectal cancer screening. Patients in the intervention and control group were similar for both the patient-level and physician-level randomizations, except for a nonsignificant trend (P = .08) toward more office visits in the control group for the physician intervention (Table 1). The mean (SD) age of physicians was 48 (9.7) years, and 57% were female. Their mean (SD) number of eligible patients aged 50 to 80 was 199 (95), with no differences according to intervention status.

Table Graphic Jump LocationTable 1. Baseline Patient Characteristics
SCREENING RATES

Among this group of patients who were overdue for screening with usual care, patients who received the mailing were significantly more likely to complete colorectal cancer screening than those who did not (44.0% vs 38.1%; P < .001). The patient mailing was more effective among older patients, with the absolute increase in screening rates ranging from 3.7% among patients aged 50 to 59 years to 10.1% among patients aged 70 to 80 (P = .01 for trend) (Table 2). The impact of the mailing did not differ between women and men (Table 2). The mailing primarily increased the performance of FOBT among the intervention group compared with the control group (25.4% vs 20.4%; P < .001) (Table 3). Among patients with a positive FOBT result, 73% of this group overall underwent subsequent colonoscopy, with no significant differences by patient or physician intervention group (Table 3).

Table Graphic Jump LocationTable 2. Receipt of Colorectal Cancer Screening by Intervention Status
Table Graphic Jump LocationTable 3. Types of Colorectal Cancer Screening Tests and Pathologic Findings by Intervention Status

Patients whose physicians received electronic reminders during the study period were not more likely than patients whose physicians did not receive reminders to complete colorectal screening (41.9% vs 40.2%; P = .47), but among patients with 3 or more primary care visits, reminders tended to increase screening rates (59.5% vs 52.7%; P = .07) (Table 2). Although the overall screening rate and rate of completed colonoscopies did not increase significantly with physician reminders, these electronic reminders did increase the proportion of patients who had an order for colonoscopy placed during the study period (33.1% vs 29.6%; P = .004). In contrast, colonoscopy orders did not increase significantly for patients who received mailed reminders (31.8% vs 30.9%; P = .12). Among all patients who completed a colonoscopy, the median time from ordering to completion of this test was 49 days (interquartile range, 27-85 days), suggesting adequate capacity for this procedure and acceptable waiting times.

The screening rate among patients who received mailed reminders and whose physicians received electronic reminders was 44.2%, compared with 43.7% for those in the patient intervention but not the physician intervention, 39.6% for those in the physician intervention but not the patient intervention, and 36.7% for those in neither intervention group. The interaction between the patient intervention and the physician intervention was small, negative, and not statistically significant (−0.6%; 95% CI, −1.2% to 0.1%) (P = .08), indicating that the observed effect of the combined patient and physician reminders was 0.6% less than the sum of their effects when applied individually

DETECTION OF ADENOMAS AND CANCERS

Detection of colorectal adenomas tended to be greater among patients who received mailings (5.7% vs 5.2%; P = .10) and among patients of physicians receiving electronic reminders compared with the respective control groups (6.0% vs 4.9%; P = .09) (Table 3). Among patients with adenomas, 15% had 3 or more adenomas removed, 8% had an adenoma 10 mm or greater in diameter, 1% had villous histologic features, and 23% had at least 1 of these high-risk features. Overall, 34 patients (0.2%) were newly diagnosed as having colorectal cancer, with no significant differences between intervention groups (Table 3). Among these 34 incident colorectal cancers, 56% were diagnosed at an early stage (stage 0, 1, or 2), 35% were diagnosed at a later stage (stages 3 or 4), and 9% lacked definitive stage data.

PHYSICIAN SURVEY

Of 43 eligible physicians, 33 (77%) in the intervention group completed the survey. Nearly all (97%) physicians considered colonoscopy every 10 years to be “very effective” at reducing colorectal cancer mortality, while only 3% perceived an annual FOBT as similarly effective. Accordingly, all respondents (100%) reported colonoscopy as the screening test they most often recommended to patients. Physicians reported that electronic reminders accurately reflected their patients' screening status for a median of 50% of the reminders (interquartile range, 30%-80%). Most physicians in the intervention group reported that the electronic reminders were “very effective” (9%) or “somewhat effective” (47%) in increasing the colorectal screening rate among their patients.

In a large cohort of patients who were overdue for screening, we demonstrated that personalized mailings to individual patients produced a modest increase in colorectal cancer screening, particularly by FOBT and among patients in the oldest age group, suggesting that patients represent an untapped resource for improving quality of care. Patients frequently report that they have not received effective counseling regarding the importance of colorectal cancer screening.11,34 However, once eligible patients are appropriately informed, most opt to be screened for colorectal cancer.35,36 Our findings underscore that informed patients can play an active role in completing effective preventive services.37

Electronic reminders to physicians did not significantly increase overall screening rates, in part because over one-third of patients had no visits with their primary care physicians during the 15-month study period. However, physician reminders exhibited a trend toward increased overall screening rates among patients with at least 3 primary care visits over this period. Orders for colonoscopy were modestly increased with reminders to physicians but without a corresponding increase in completed procedures, as nearly half of the patients for whom a colonoscopy was ordered did not complete this procedure. This finding underscores the need for more effective communication with patients to encourage them to complete colonoscopy procedures that are scheduled.38,39

The limited effectiveness of our electronic physician reminders may reflect the challenges primary care physicians face in providing adequate preventive counseling amid competing demands during brief office visits.12 We provided “active” alerts that required physicians to respond,40 but some physicians may have disregarded the alerts if they disrupted their work flow or were deemed inaccurate.41 Although we validated the accuracy of our algorithm for detecting whether patients were up-to-date with screening, many physicians considered the electronic reminders as substantially less accurate, and nearly half of the physicians considered the reminders as ineffective. This suggests that further collaboration with the practicing physicians who receive reminders via electronic health records may be required to achieve a greater impact on screening rates.

Our study highlights an important contrast between the screening strategy pursued by patients and the preferences of their physicians. The patient mailings produced a modest increase in the use of FOBT, but all physicians considered colonoscopy as the preferred screening test for their patients. This finding is consistent with recent studies indicating a preference for FOBT over colonoscopy among patients who were provided information to make an informed choice,42 whereas physicians report a strong preference to recommend colonoscopy.43 This contrast highlights 1 potential challenge to engaging patients in quality-improvement programs. For services such as colorectal cancer screening for which multiple reasonable options exist, quality-improvement programs will need to address the possibly differing preferences of patients and their physicians and develop methods to reconcile such differences.44,45

Increased screening is essential to reduce the incidence, morbidity, and mortality of colorectal cancer. One recent study estimated that US mortality from this disease could be reduced 23% by 2020 if screening rates rose to 70%.46 The importance of colorectal cancer screening has been recognized through expanded Medicare coverage for this service in 200147 and the endorsement of colorectal cancer screening as a health plan performance measure by the National Committee for Quality Assurance in 2005.48 Published studies of interventions to improve rates of colorectal cancer screening have targeted patients, physicians, or both groups.14,15,1728 Physician-directed interventions such as reminders16,23,24,28 and performance feedback25 have increased screening rates in some settings. Patient-directed interventions including videotaped decision aids,19 educational mailings,20,21 and nurse counseling18 may also increase screening rates.

Our randomized trial builds on these studies in several important ways. First, these prior studies typically occurred in settings where baseline screening rates were much lower than the screening rate of 63% in our population, often produced larger absolute increases in screening rates, and focused on increasing use of FOBT or flexible sigmoidoscopy. These studies may not apply to the current era in which screening rates are higher and colonoscopy has become a preferred screening strategy among physicians43 and is therefore increasingly used.47 In fact, more recent interventions that have included use of colonoscopy in their recommendations have not successfully increased overall screening rates.22,26,27

Our study provides important insights into the effect of interventions focused on patients who remain unscreened as screening rates rise through usual care. First, the modest effect of patient reminders in our study suggests the need to develop more effective strategies to actively engage these remaining patients and encourage them to be screened for colorectal cancer. However, the clear advantage of patient involvement over physician reminders in our study suggests that future strategies should increasingly involve patient-based activity. Promising alternatives include the use of the Internet to facilitate patient-provider communication and promote increased patient involvement in their preventive health issues.49 Patient navigators have also been used with success in promoting cancer screening, particularly among low-income and minority groups.50

Second, our intervention simultaneously evaluated the use of personalized mailings to patients and electronic reminders to physicians. We found that patient mailings were more effective than physician reminders in raising overall screening rates, and nonsignificant trends in detection of colorectal adenomas were evident with each approach. Involving patients in decisions about colorectal cancer screening fits well with models that promote informed patients,37 moving them through the “stages of decision,” from awareness of screening options through the decision to be screened.19,5153 Third, our large sample and rigorous study design allowed reasonably precise estimates of the intervention effects.

Fourth, the use of data from electronic medical records provided relatively complete clinical information on this large patient population, including data on clinical processes and outcomes. Approximately three-quarters of the positive FOBT results in our study population were followed by a colonoscopy. Although closing this loop is essential to realizing the benefits of a screening program,54 many studies demonstrate a similar gap in care.5563 Physicians may not recommend appropriate follow-up testing to patients,56,57,62 patients may refuse further testing,57 or appropriate systems may not be in place to help clinicians identify abnormal test results and ensure appropriate follow-up.63

The generalizability of our study must also be considered. We implemented our intervention within a single group practice using an advanced electronic health record, so our findings may not apply to less structured settings. In particular, integrated medical groups generally provide higher-quality care for screening services.27,64 However, our patient mailing intervention could be implemented across a wide range of health care settings, and the adoption of electronic health records is being actively promoted to improve ambulatory care.65 Our study demonstrated how electronic data can be used to create clinical registries for outreach to patients, and it assessed the utility of decision support that is directly integrated with computerized order entry for physicians providing ambulatory care. After our study found that the patient mailings were effective, the integrated group practice instituted a routine protocol to identify patients overdue for colorectal cancer screening (including patients in our control group) and send them mailings regarding their need for screening.

In conclusion, this randomized trial of personalized patient mailings and electronic reminders to physicians in a large integrated group practice found that patient mailings produced modest increases in rates of colorectal cancer screening, whereas electronic physician reminders tended to promote screening only among patients who have more frequent primary care visits. These complementary approaches have the potential to promote the overarching goal of widespread screening to reduce the incidence, morbidity, and mortality of colorectal cancer.

Correspondence: John Z. Ayanian, MD, MPP, Department of Health Care Policy, Harvard Medical School, 180 Longwood Ave, Boston, MA 02115 (ayanian@hcp.med.harvard.edu).

Accepted for Publication: September 22, 2008.

Author Contributions:Study concept and design: Sequist, Marshall, Fletcher, and Ayanian. Acquisition of data: Sequist, Marshall, and Ayanian. Analysis and interpretation of data: Sequist, Zaslavsky, Marshall, Fletcher, and Ayanian. Drafting of the manuscript: Sequist, Fletcher, and Ayanian. Critical revision of the manuscript for important intellectual content: Sequist, Zaslavsky, Marshall, Fletcher, and Ayanian. Statistical analysis: Sequist, Zaslavsky, and Ayanian. Obtained funding: Sequist and Ayanian. Administrative, technical, and material support: Sequist, Marshall, and Fletcher. Study supervision: Ayanian.

Financial Disclosure: None reported.

Funding/Support: The study was funded by grant R01 CA112367 from the National Cancer Institute.

Role of the Sponsor: The funder played no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; or preparation, review, and approval of the manuscript.

Previous Presentation: This study was presented at the 2008 Society of General Internal Medicine Annual Meeting; April 10, 2008; Pittsburgh, Pennsylvania.

Additional Contributions: We are grateful to the patients and physicians of Harvard Vanguard Medical Associates for their participation in this study. J. Alan Kemp, MD, provided advice on the study design; Jo-Anne Foley, Rebecca Lobb, Amy Marston, and Debby Collins assisted with project management; Robert Wolf and James Morrissey provided data management and analysis; Aimee Shu, MD, and Jeffrey Kullgren, MD, MPH, reviewed medical records.

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Beydoun  HABeydoun  MA Predictors of colorectal cancer screening behaviors among average-risk older adults in the United States. Cancer Causes Control 2008;19 (4) 339- 359
PubMed Link to Article
Zapka  JGPuleo  EVickers-Lahti  MLuckmann  R Healthcare system factors and colorectal cancer screening. Am J Prev Med 2002;23 (1) 28- 35
PubMed Link to Article
Zarychanski  RChen  YBernstein  CNHebert  PC Frequency of colorectal cancer screening and the impact of family physicians on screening behaviour. CMAJ 2007;177 (6) 593- 597
PubMed Link to Article
Wee  CC McCarthy  EPPhillips  RS Factors associated with colon cancer screening: the role of patient factors and physician counseling. Prev Med 2005;41 (1) 23- 29
PubMed Link to Article
Leard  LESavides  TJGaniats  TG Patient preferences for colorectal cancer screening. J Fam Pract 1997;45 (3) 211- 218
PubMed
Pignone  MBucholtz  DHarris  R Patient preferences for colon cancer screening. J Gen Intern Med 1999;14 (7) 432- 437
PubMed Link to Article
Bodenheimer  T Wagner  EHGrumbach  K Improving primary care for patients with chronic illness: the chronic care model, part 2. JAMA 2002;288 (15) 1909- 1914
PubMed Link to Article
Denberg  TDCoombes  JMByers  TE  et al.  Effect of a mailed brochure on appointment-keeping for screening colonoscopy: a randomized trial. Ann Intern Med 2006;145 (12) 895- 900
PubMed Link to Article
Turner  BJWeiner  MBerry  SDLillie  KFosnocht  KHollenbeak  CS Overcoming poor attendance to first scheduled colonoscopy: a randomized trial of peer coach or brochure support. J Gen Intern Med 2008;23 (1) 58- 63
PubMed Link to Article
Litzelman  DKDittus  RSMiller  METierney  WM Requiring physicians to respond to computerized reminders improves their compliance with preventive care protocols. J Gen Intern Med 1993;8 (6) 311- 317
PubMed Link to Article
Ash  JSBerg  MCoiera  E Some unintended consequences of information technology in health care: the nature of patient care information system-related errors. J Am Med Inform Assoc 2004;11 (2) 104- 112
PubMed Link to Article
DeBourcy  ACLichtenberger  SFelton  SButterfield  KTAhnen  DJDenberg  TD Community-based preferences for stool cards versus colonoscopy in colorectal cancer screening. J Gen Intern Med 2008;23 (2) 169- 174
PubMed Link to Article
Klabunde  CNFrame  PSMeadow  AJones  ENadel  MVernon  SW A national survey of primary care physicians' colorectal cancer screening recommendations and practices. Prev Med 2003;36 (3) 352- 362
PubMed Link to Article
Klabunde  CNLanier  DBreslau  ES  et al.  Improving colorectal cancer screening in primary care practice: innovative strategies and future directions. J Gen Intern Med 2007;22 (8) 1195- 1205
PubMed Link to Article
Lafata  JEDivine  GMoon  CWilliams  LK Patient-physician colorectal cancer screening discussions and screening use. Am J Prev Med 2006;31 (3) 202- 209
PubMed Link to Article
Vogelaar  Ivan Ballegooijen  MSchrag  D  et al.  How much can current interventions reduce colorectal cancer mortality in the US? mortality projections for scenarios of risk-factor modification, screening, and treatment. Cancer 2006;107 (7) 1624- 1633
PubMed Link to Article
Gross  CPAndersen  MSKrumholz  HM McAvay  GJProctor  DTinetti  ME Relation between Medicare screening reimbursement and stage at diagnosis for older patients with colon cancer. JAMA 2006;296 (23) 2815- 2822
PubMed Link to Article
Schneider  ECNadel  MRZaslavsky  AM McGlynn  EA Assessment of the Scientific Soundness of Clinical Performance Measures: a Field Test of the National Committee for Quality Assurance's Colorectal Cancer Screening Measure. Arch Intern Med 2008;168 (8) 876- 882
PubMed Link to Article
Poon  EGWald  JSchnipper  JL  et al.  Empowering patients to improve the quality of their care: design and implementation of a shared health maintenance module in a US integrated healthcare delivery network. Stud Health Technol Inform 2007;129 (pt 2) 1002- 1006
PubMed
Christie  JItzkowitz  SLihau-Nkanza  ICastillo  ARedd  WJandorf  L A randomized controlled trial using patient navigation to increase colonoscopy screening among low-income minorities. J Natl Med Assoc 2008;100 (3) 278- 284
PubMed
Prochaska  JODiClemente  CC Stages and processes of self-change of smoking: toward an integrative model of change. J Consult Clin Psychol 1983;51 (3) 390- 395
PubMed Link to Article
Sarfaty  MWender  R How to increase colorectal cancer screening rates in practice. CA Cancer J Clin 2007;57 (6) 354- 366
PubMed Link to Article
Arora  NKAyanian  JZGuadagnoli  E Examining the relationship of patients' attitudes and beliefs with their self-reported level of participation in medical decision-making. Med Care 2005;43 (9) 865- 872
PubMed Link to Article
Yabroff  KRWashington  KSLeader  ANeilson  EMandelblatt  J Is the promise of cancer-screening programs being compromised? quality of follow-up care after abnormal screening results. Med Care Res Rev 2003;60 (3) 294- 331
PubMed Link to Article
Levin  BHess  KJohnson  C Screening for colorectal cancer: a comparison of 3 fecal occult blood tests. Arch Intern Med 1997;157 (9) 970- 976
PubMed Link to Article
Shields  HMWeiner  MSHenry  DR  et al.  Factors that influence the decision to do an adequate evaluation of a patient with a positive stool for occult blood. Am J Gastroenterol 2001;96 (1) 196- 203
PubMed Link to Article
Baig  NMyers  RETurner  BJ  et al.  Physician-reported reasons for limited follow-up of patients with a positive fecal occult blood test screening result. Am J Gastroenterol 2003;98 (9) 2078- 2081
PubMed Link to Article
Turner  BMyers  REHyslop  T  et al.  Physician and patient factors associated with ordering a colon evaluation after a positive fecal occult blood test. J Gen Intern Med 2003;18 (5) 357- 363
PubMed Link to Article
Etzioni  DAYano  EMRubenstein  LV  et al.  Measuring the quality of colorectal cancer screening: the importance of follow-up. Dis Colon Rectum 2006;49 (7) 1002- 1010
PubMed Link to Article
Fisher  DAJeffreys  ACoffman  CJFasanella  K Barriers to full colon evaluation for a positive fecal occult blood test. Cancer Epidemiol Biomarkers Prev 2006;15 (6) 1232- 1235
PubMed Link to Article
Lurie  JDWelch  HG Diagnostic testing following fecal occult blood screening in the elderly. J Natl Cancer Inst 1999;91 (19) 1641- 1646
PubMed Link to Article
Nadel  MRShapiro  JAKlabunde  CN  et al.  A national survey of primary care physicians' methods for screening for fecal occult blood. Ann Intern Med 2005;142 (2) 86- 94
PubMed Link to Article
Klabunde  CNRiley  GFMandelson  MTFrame  PSBrown  ML Health plan policies and programs for colorectal cancer screening: a national profile. Am J Manag Care 2004;10 (4) 273- 279
PubMed
Mehrotra  AEpstein  AMRosenthal  MB Do integrated medical groups provide higher-quality medical care than individual practice associations? Ann Intern Med 2006;145 (11) 826- 833
PubMed Link to Article
Bates  DW Physicians and ambulatory electronic health records US physicians are ready to make the transition to EHRs—which is clearly overdue, given the rest of the world's experience. Health Aff (Millwood) 2005;24 (5) 1180- 1189
PubMed Link to Article

Figures

Place holder to copy figure label and caption
Figure 1.

CONSORT (Consolidated Standards of Reporting Trials) diagram of patient and physician eligibility and randomization. For the patient mailing, patients were randomized within physician panels, and for the electronic reminders, physicians were randomized within each health center.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 2.

Active electronic reminders were delivered to physicians during office encounters and facilitated electronic ordering of recommended tests.

Graphic Jump Location

Tables

Table Graphic Jump LocationTable 1. Baseline Patient Characteristics
Table Graphic Jump LocationTable 2. Receipt of Colorectal Cancer Screening by Intervention Status
Table Graphic Jump LocationTable 3. Types of Colorectal Cancer Screening Tests and Pathologic Findings by Intervention Status

References

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Klabunde  CNVernon  SWNadel  MRBreen  NSeeff  LCBrown  ML Barriers to colorectal cancer screening: a comparison of reports from primary care physicians and average-risk adults. Med Care 2005;43 (9) 939- 944
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Guerra  CESchwartz  JSArmstrong  KBrown  JSHalbert  CHShea  JA Barriers of and facilitators to physician recommendation of colorectal cancer screening. J Gen Intern Med 2007;22 (12) 1681- 1688
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Turner  BJDay  SCBorenstein  B A controlled trial to improve delivery of preventive care: physician or patient reminders? J Gen Intern Med 1989;4 (5) 403- 409
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Pignone  MHarris  RKinsinger  L Videotape-based decision aid for colon cancer screening: a randomized, controlled trial. Ann Intern Med 2000;133 (10) 761- 769
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Church  TRYeazel  MWJones  RM  et al.  A randomized trial of direct mailing of fecal occult blood tests to increase colorectal cancer screening. J Natl Cancer Inst 2004;96 (10) 770- 780
PubMed Link to Article
Zapka  JGLemon  SCPuleo  EEstabrook  BLuckmann  RErban  S Patient education for colon cancer screening: a randomized trial of a video mailed before a physical examination. Ann Intern Med 2004;141 (9) 683- 692
PubMed Link to Article
Balas  EAWeingarten  SGarb  CTBlumenthal  DBoren  SABrown  GD Improving preventive care by prompting physicians. Arch Intern Med 2000;160 (3) 301- 308
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Shea  SDuMouchel  WBahamonde  L A meta-analysis of 16 randomized controlled trials to evaluate computer-based clinical reminder systems for preventive care in the ambulatory setting. J Am Med Inform Assoc 1996;3 (6) 399- 409
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Ferreira  MRDolan  NCFitzgibbon  ML  et al.  Health care provider-directed intervention to increase colorectal cancer screening among veterans: results of a randomized controlled trial. J Clin Oncol 2005;23 (7) 1548- 1554
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Walsh  JMSalazar  RTerdiman  JPGildengorin  GPerez-Stable  EJ Promoting use of colorectal cancer screening tests: can we change physician behavior? J Gen Intern Med 2005;20 (12) 1097- 1101
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Ganz  PAFarmer  MMBelman  MJ  et al.  Results of a randomized controlled trial to increase colorectal cancer screening in a managed care health plan. Cancer 2005;104 (10) 2072- 2083
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McPhee  SJBird  JAFordham  DRodnick  JEOsborn  EH Promoting cancer prevention activities by primary care physicians: results of a randomized, controlled trial. JAMA 1991;266 (4) 538- 544
PubMed Link to Article
Levin  BLieberman  DA McFarland  B  et al.  Screening and surveillance for the early detection of colorectal cancer and adenomatous polyps, 2008: a joint guideline from the American Cancer Society, the US Multi-Society Task Force on Colorectal Cancer, and the American College of Radiology. Gastroenterology 2008;134 (5) 1570- 1595
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Greene  FLPage  DLFleming  IDBalch  CMHaller  DGMorrow  M  AJCC Cancer Staging Manual.  6th ed. Philadelphia, PA Lippincott Raven2002;
Beydoun  HABeydoun  MA Predictors of colorectal cancer screening behaviors among average-risk older adults in the United States. Cancer Causes Control 2008;19 (4) 339- 359
PubMed Link to Article
Zapka  JGPuleo  EVickers-Lahti  MLuckmann  R Healthcare system factors and colorectal cancer screening. Am J Prev Med 2002;23 (1) 28- 35
PubMed Link to Article
Zarychanski  RChen  YBernstein  CNHebert  PC Frequency of colorectal cancer screening and the impact of family physicians on screening behaviour. CMAJ 2007;177 (6) 593- 597
PubMed Link to Article
Wee  CC McCarthy  EPPhillips  RS Factors associated with colon cancer screening: the role of patient factors and physician counseling. Prev Med 2005;41 (1) 23- 29
PubMed Link to Article
Leard  LESavides  TJGaniats  TG Patient preferences for colorectal cancer screening. J Fam Pract 1997;45 (3) 211- 218
PubMed
Pignone  MBucholtz  DHarris  R Patient preferences for colon cancer screening. J Gen Intern Med 1999;14 (7) 432- 437
PubMed Link to Article
Bodenheimer  T Wagner  EHGrumbach  K Improving primary care for patients with chronic illness: the chronic care model, part 2. JAMA 2002;288 (15) 1909- 1914
PubMed Link to Article
Denberg  TDCoombes  JMByers  TE  et al.  Effect of a mailed brochure on appointment-keeping for screening colonoscopy: a randomized trial. Ann Intern Med 2006;145 (12) 895- 900
PubMed Link to Article
Turner  BJWeiner  MBerry  SDLillie  KFosnocht  KHollenbeak  CS Overcoming poor attendance to first scheduled colonoscopy: a randomized trial of peer coach or brochure support. J Gen Intern Med 2008;23 (1) 58- 63
PubMed Link to Article
Litzelman  DKDittus  RSMiller  METierney  WM Requiring physicians to respond to computerized reminders improves their compliance with preventive care protocols. J Gen Intern Med 1993;8 (6) 311- 317
PubMed Link to Article
Ash  JSBerg  MCoiera  E Some unintended consequences of information technology in health care: the nature of patient care information system-related errors. J Am Med Inform Assoc 2004;11 (2) 104- 112
PubMed Link to Article
DeBourcy  ACLichtenberger  SFelton  SButterfield  KTAhnen  DJDenberg  TD Community-based preferences for stool cards versus colonoscopy in colorectal cancer screening. J Gen Intern Med 2008;23 (2) 169- 174
PubMed Link to Article
Klabunde  CNFrame  PSMeadow  AJones  ENadel  MVernon  SW A national survey of primary care physicians' colorectal cancer screening recommendations and practices. Prev Med 2003;36 (3) 352- 362
PubMed Link to Article
Klabunde  CNLanier  DBreslau  ES  et al.  Improving colorectal cancer screening in primary care practice: innovative strategies and future directions. J Gen Intern Med 2007;22 (8) 1195- 1205
PubMed Link to Article
Lafata  JEDivine  GMoon  CWilliams  LK Patient-physician colorectal cancer screening discussions and screening use. Am J Prev Med 2006;31 (3) 202- 209
PubMed Link to Article
Vogelaar  Ivan Ballegooijen  MSchrag  D  et al.  How much can current interventions reduce colorectal cancer mortality in the US? mortality projections for scenarios of risk-factor modification, screening, and treatment. Cancer 2006;107 (7) 1624- 1633
PubMed Link to Article
Gross  CPAndersen  MSKrumholz  HM McAvay  GJProctor  DTinetti  ME Relation between Medicare screening reimbursement and stage at diagnosis for older patients with colon cancer. JAMA 2006;296 (23) 2815- 2822
PubMed Link to Article
Schneider  ECNadel  MRZaslavsky  AM McGlynn  EA Assessment of the Scientific Soundness of Clinical Performance Measures: a Field Test of the National Committee for Quality Assurance's Colorectal Cancer Screening Measure. Arch Intern Med 2008;168 (8) 876- 882
PubMed Link to Article
Poon  EGWald  JSchnipper  JL  et al.  Empowering patients to improve the quality of their care: design and implementation of a shared health maintenance module in a US integrated healthcare delivery network. Stud Health Technol Inform 2007;129 (pt 2) 1002- 1006
PubMed
Christie  JItzkowitz  SLihau-Nkanza  ICastillo  ARedd  WJandorf  L A randomized controlled trial using patient navigation to increase colonoscopy screening among low-income minorities. J Natl Med Assoc 2008;100 (3) 278- 284
PubMed
Prochaska  JODiClemente  CC Stages and processes of self-change of smoking: toward an integrative model of change. J Consult Clin Psychol 1983;51 (3) 390- 395
PubMed Link to Article
Sarfaty  MWender  R How to increase colorectal cancer screening rates in practice. CA Cancer J Clin 2007;57 (6) 354- 366
PubMed Link to Article
Arora  NKAyanian  JZGuadagnoli  E Examining the relationship of patients' attitudes and beliefs with their self-reported level of participation in medical decision-making. Med Care 2005;43 (9) 865- 872
PubMed Link to Article
Yabroff  KRWashington  KSLeader  ANeilson  EMandelblatt  J Is the promise of cancer-screening programs being compromised? quality of follow-up care after abnormal screening results. Med Care Res Rev 2003;60 (3) 294- 331
PubMed Link to Article
Levin  BHess  KJohnson  C Screening for colorectal cancer: a comparison of 3 fecal occult blood tests. Arch Intern Med 1997;157 (9) 970- 976
PubMed Link to Article
Shields  HMWeiner  MSHenry  DR  et al.  Factors that influence the decision to do an adequate evaluation of a patient with a positive stool for occult blood. Am J Gastroenterol 2001;96 (1) 196- 203
PubMed Link to Article
Baig  NMyers  RETurner  BJ  et al.  Physician-reported reasons for limited follow-up of patients with a positive fecal occult blood test screening result. Am J Gastroenterol 2003;98 (9) 2078- 2081
PubMed Link to Article
Turner  BMyers  REHyslop  T  et al.  Physician and patient factors associated with ordering a colon evaluation after a positive fecal occult blood test. J Gen Intern Med 2003;18 (5) 357- 363
PubMed Link to Article
Etzioni  DAYano  EMRubenstein  LV  et al.  Measuring the quality of colorectal cancer screening: the importance of follow-up. Dis Colon Rectum 2006;49 (7) 1002- 1010
PubMed Link to Article
Fisher  DAJeffreys  ACoffman  CJFasanella  K Barriers to full colon evaluation for a positive fecal occult blood test. Cancer Epidemiol Biomarkers Prev 2006;15 (6) 1232- 1235
PubMed Link to Article
Lurie  JDWelch  HG Diagnostic testing following fecal occult blood screening in the elderly. J Natl Cancer Inst 1999;91 (19) 1641- 1646
PubMed Link to Article
Nadel  MRShapiro  JAKlabunde  CN  et al.  A national survey of primary care physicians' methods for screening for fecal occult blood. Ann Intern Med 2005;142 (2) 86- 94
PubMed Link to Article
Klabunde  CNRiley  GFMandelson  MTFrame  PSBrown  ML Health plan policies and programs for colorectal cancer screening: a national profile. Am J Manag Care 2004;10 (4) 273- 279
PubMed
Mehrotra  AEpstein  AMRosenthal  MB Do integrated medical groups provide higher-quality medical care than individual practice associations? Ann Intern Med 2006;145 (11) 826- 833
PubMed Link to Article
Bates  DW Physicians and ambulatory electronic health records US physicians are ready to make the transition to EHRs—which is clearly overdue, given the rest of the world's experience. Health Aff (Millwood) 2005;24 (5) 1180- 1189
PubMed Link to Article

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