Colorectal Cancer Screening Use Among Insured Primary Care Patients

Objective: To compare colorectal cancer (CRC) screening use, including changes over time and demographic characteristics associated with screening receipt, between 2 insured primary care populations.

Study Design: Clinical and administrative records from 2 large health systems, one in New Mexico and the other in Michigan, were used to determine use of CRC screening tests between 2004 and 2008 among patients aged 51 to 74 years.

Methods: Generalized estimating equations were used to evaluate trends in CRC screening use over time and the association of demographic and other factors with screening receipt.

Results: Rates of CRC screening use ranged from 48.1% at the New Mexico site to 68.7% at the Michigan site, with colonoscopy being the most frequently used modality. Fecal occult blood test was used inconsistently by substantial proportions of patients who did not meet the definition of screening users. Screening use was positively

and significantly associated with older age, male sex, and more periodic health examinations and other types of primary care visits; at the Michigan site, it was also associated with African American race, married status, and higher annual estimated household income.

Conclusions: Among insured primary care patients, CRC screening use falls short. Further research is needed to determine what factors are barriers to routine fecal occult blood test or colonoscopy use among insured patients who have access to and regularly use primary care and how those barriers can be eliminated.

(Am J Manag Care. 2011;17(7):480-488)

Commonalities in colorectal cancer screening use were evident across 2 insured primary care populations.

• Between one-third and one-half of patients at each site were not up-to-date with screening.

• At both sites, younger patients, female patients, and patients with fewer periodic health examinations and other types of primary care visits were at greater risk of being unscreened for colorectal cancer.

• Among recommended testing modalities, colonoscopy was by far the most used test among patients who were up-to-date with screening.

• Although fecal occult blood test use was common, adherence to annual testing was a challenge at both sites.

Colorectal cancer (CRC) screening was first recommended by professional organizations for average-risk adults 50 years and older more than 2 decades ago.^1-5 Most recently, the US Preventive Services Task Force⁴ issued evidence-based CRC screening guidelines recommending the use of the following: (1) fecal occult blood test (FOBT) or fecal immunochemical test annually, (2) FOBT or fecal immunochemical test every 3 years combined with flexible sigmoidoscopy every 5 years, or (3) colonoscopy every 10 years. Despite these guidelines and the availability of several effective screening tests, CRC screening remains underused.

Population-based surveys indicate that CRC screening rates have increased steadily over time,^6-8 with the most recent estimates showing that screening rates exceed 60%.^7,9 Less recently, claims-based and medical record—based studies among insured populations point to similar trends but tend to place estimates of the screened population somewhat below those obtained by self-report^10,11 and indicate an increase in the use of colonoscopy relative to other modalities.^12,13

Using automated claims and electronic medical record data for a 5-year period ending December 31, 2008, we compared CRC screening use between insured primary care populations receiving care from 2 large integrated delivery systems, one located in southeast Michigan and the other located in central New Mexico. We report annual screening use by modality between 2004 and 2008 and examine demographic and other patient factors associated with screening receipt.

METHODS

Study Settings and Samples

Eligible patient populations were selected from those receiving primary care at 2 health systems. The Michigan health system includes a 900-member multispecialty salaried medical group that staffs 27 primary care clinics in Detroit and surrounding communities. The New Mexico health system is the largest physician-owned multispecialty physician group in the state, with 230 salaried physicians and 70 midlevel care providers. It staffs 10 primary care clinics in Albuquerque and surrounding communities. Both sites are participating in a Centers for Disease Control and Prevention—sponsored randomized controlled trial evaluating an intervention to increase CRC screening among primary care patients. These 2 health systems were chosen for trial participation because they have a large number of eligible patients and

physicians, a high proportion of minority patients, and strong research capacity and data capture capabilities.

Patients eligible for study inclusion were those aged 51 to 74 years on December 31, 2008, and continuously enrolled in a system-affiliated health maintenance organization during the 5-year study period ending December 31, 2008 (ie, the 5-year period preceding intervention implementation). To our knowledge, no randomized controlled trials to increase CRC screening took place at either health system during the study period. All patients with health plan enrollment were eligible regardless of whether their coverage was sponsored by employer, Medicare, or other. Although Michigan patients had copayments for office visits, they had no cost sharing specific to CRC screening tests. New Mexico patients may have had a deductible, minimal copayment, or both for endoscopy procedures depending on their personal coverage and situation. Eligible study patients also had at least 1 primary care visit during the study period (2004-2008). Exclusion criteria included evidence of a history of colorectal carcinoma, ulcerative colitis, Crohn’s disease, or bowel resection. The study was approved by the institutional review board at each participating site.

Data Sources and Measures

Automated health system records were used to obtain patient age, sex, race (Michigan site only) or ethnicity (New Mexico site only), residential street address, marital status (Michigan site only), primary care visit frequency, diagnoses, and receipt of CRC screening tests. At the Michigan site, race is recorded as 1 ethnicity was determined using GUESS (Generally Useful Ethnicity Search System), which identifies ethnicity based on surname. GUESS has been shown to be 90% accurate for identifying individuals of Hispanic ethnicity in New Mexico.¹⁴

Residential street address was combined with zip code—level data for 2009 from the Current Population Survey to construct an annual estimated household income for patients.¹⁵ Inpatient and outpatient International Classification of Diseases, Ninth Revision, Clinical Modification diagnostic codes during the 5-year period were used to construct an adapted Charlson Comorbidity Index.¹⁶ Current Procedural Terminology codes were used to categorize primary care visits during the 5-year period as periodic health examinations (PHEs) or as other types of primary care visits.

We calculated annual testing rates for FOBT, colonoscopy, flexible sigmoidoscopy, double-contrast barium enema, combination of FOBT and flexible sigmoidoscopy, and other modality combinations for 2004 through 2008. Five-year CRC screening receipt was based on the 2002 US Preventive Services Task Force guidelines.¹⁷ Patients who received at least 3 FOBTs (>10 months apart) or 1 colonoscopy, flexible sigmoidoscopy, or double-contrast barium enema during the 5-year period were considered screening users. Patients with evidence of colonoscopy receipt between 1999 and 2003 were also considered screening users.

Statistical Analysis

Characteristics of patients receiving care from the 2 health systems were compared using X² test for differences in proportions, t test for differences in age, and Wilcoxon rank sum test for differences in annual estimated household income and primary care visit frequency. For the analysis of time effects, year was represented by 4 indicator variables, and an overall 4-df test for year effect was performed. For analyses of withinsystem effects, generalized estimating equation logistic regression models were used to account for the nesting of patients receiving care from the same primary care provider. For differences in screening use by patient characteristics, generalized

estimating equation logistic regression models were used for each characteristic by itself and after adjustment for patient age, sex, race/ethnicity, annual estimated household income, frequency of PHEs and other types of primary care visits, and Charlson Comorbidity Index. The Michigan health system models were also adjusted for marital status.

RESULTS

Cohort Characteristics

In Michigan, 13.5% of the cohort were older than 65 years, and 54.1% were female (Table 1). Approximately one-third of patients (37.1%) were African American. Most patients (73.4%) were married, and the mean annual estimated house-communities of residence was $76,846. Sixty-three percent of patients had at least 1 PHE during the study period, and 37.0% had at least 2 PHEs in the 5-year period. Compared with Michigan patients, New Mexico patients were significantly older (P <.01) and were more likely to be female, reside in areas with lower annual estimated household income, and have fewer primary care visits. hold income in their communities of residence was $89,809. Most patients (63.4%) had at least 1 PHE during the study period (2004-2008), with 44.0% having at least 2 such visits.

In New Mexico, 46.8% of patients were older than 65 years, and 57.0% were female, while approximately one-third of patients (36.2%) were of Hispanic ethnicity (Table 1). The mean annual estimated household income in their communities of residence was $76,846. Sixty-three percent of patients had at least 1 PHE during the study period, and 37.0% had at least 2 PHEs in the 5-year period. Compared with Michigan patients, New Mexico patients were significantly older (P <.01) and were more likely to be female, reside in areas with lower annual estimated household income, and have fewer primary care visits.

Annual CRC Screening Use

As summarized in Table 2, annual CRC screening use (overall and for specific modalities) varied by year at both sites (P <.01 for all). At the Michigan site, the overall annual CRC screening rate increased steadily between 2004 and 2008. Annual use of colonoscopy increased between 2004 and 2007, and annual use of FOBT increased between 2005 and 2008. At the New Mexico site, the overall annual CRC screening rate increased between 2004 and 2005 and declined thereafter. Annual colonoscopy and FOBT use among New Mexico patients paralleled this overall pattern. At both health systems, only the use of colonoscopy alone or FOBT alone contributed substantively to the observed annual use of screening.

Five-Year CRC Screening Use

Sixty-nine percent of the Michigan cohort and 48.1% of the New Mexico cohort met the criteria for screening users (Table 3). Most users were screened during the 5-year study period, but 9.3% of Michigan patients and 8.7% of New Mexico patients were classified as screening users based on evidence of colonoscopy receipt during the 5 years preceding the study period. Among patients who met the criteria for screening users, colonoscopy was the most frequently used screening modality; almost 90% of users at each health system met the definition of screening users because of their receipt of a colonoscopy. Regardless of health system, the use of each of the other recommended screening modalities was rare, including repeated use of FOBT (>3) alone or in combination with flexible sigmoidoscopy. Among patients who did not meet the criteria for screening users in the 5-year study period, 22.5% of Michigan patients and 43.7% of New Mexico patients had 1 or 2 (but not >3) FOBTs (data not shown).

Patient Factors Associated With CRC Screening Use

At the Michigan site, CRC screening users were significantly more likely to be male (46.9% vs 43.6%), African American (37.4% vs 36.5%), and married (74.9% vs 70.0%)

compared with nonusers (Table 4). Compared with nonusers, screening users were significantly older; 38.7% of users were older than 60 years compared with 29.4% of nonusers. Users were also more likely to reside in communities with higher median annual estimated household income ($90,489 vs $88,318), receive more frequent PHEs and other types of primary care visits, and have more comorbidities as measured by the Charlson Comorbidity Index (1.1 vs 0.9). A similar pattern of significant unadjusted differences was found between CRC screening users and nonusers at the New Mexico site, with 2 exceptions: in New Mexico, there were no significant differences by sex, and patients of Hispanic ethnicity were significantly less likely to have been screened (34.5% vs 37.9%).

Among screening nonusers, approximately half (49.1% at the Michigan site and 55.6% at the New Mexico site) had at least 1 PHE during the study period, and approximately onethird had at least 2 PHEs. Almost 12% at the Michigan site and 13.6% at the New Mexico site had 3 or more PHEs during the 5-year period yet remained unscreened. Furthermore, among patients who did not meet the definition of screening users, the mean numbers of other types of primary care visits during the 5-year period were 8.5 (Michigan) and 9.1 (New Mexico) (data not shown). Among patients who completed 1 or 2 FOBTs but not 3 or more (and thus did not meet the criteria for screening users), the mean numbers of other types of primary care visits during the study period were 9.8 at the Michigan site and 9.6 at the New Mexico site (data not shown).

When patient factors were simultaneously controlled, screening use was positively and significantly associated with older age, male sex, and more PHEs and other types of primary care visits at both sites (Table 5). At the Michigan site, African American race, married status, and higher annual estimated household income were also positively associated with screening use. Patients aged 56 to 65 years at the Michigan site were approximately 50% more likely to have been screened for CRC compared with those aged 51 to 55 years, and patients aged 66 to 74 years were more than 60% more likely to have been screened compared with those aged 51 to 55 years. At the New Mexico site, the difference was most pronounced for those aged 71 to 74 years, who were almost 90% more likely to have been screened for CRC compared with those aged 51 to 55 years. Increases in PHE frequency were also associated with dramatic increases in the likelihood of screening. At the Michigan site, patients who had 3 PHEs

during the 5-year period were 4.5 times more likely to have been screened compared with patients who did not have a PHE. At the New Mexico site, patients who had 3 PHEs during the 5-year period were 2.6 times more likely to have been screened compared with patients who did not have a PHE.

DISCUSSION

Although we found that overall screening trends differed at the 2 health systems studied, with an increase in screening over time at the Michigan site and an initial increase and then a decrease at the New Mexico site, we found remarkable similarities in modality use and in patient factors associated with CRC screening use. Among both populations, most CRC screening users were recipients of colonoscopy. Yet in any given year during the study period, sizable proportions of patients used FOBT screening at both sites. Likewise, although we found a strong positive association between primary care visit frequency (particularly PHEs) and CRC screening use, we also found that substantial proportions of patients who did not meet the criteria for screening users had 2 or more PHEs over the 5-year period. These findings point to considerable

opportunities to improve CRC screening rates among insured primary care populations.

Our findings that almost 90% of CRC screening users met the definition of screening users by having received a colonoscopy are consistent with results of other medical record and claims reviews.^12,13 Such evidence is consistent with data from a national survey of physicians demonstrating that almost all physicians recommend colonoscopy to average-risk patients, in many cases as the only screening option.¹⁸ Observational studies,^19,20 including research conducted at the Michigan site studied herein, showed that CRC screening discussions in primary care tend to focus on colonoscopy. However, such practice is inconsistent with studies that point to variation

among patient preferences for CRC screening modalities. For example, a study by Hawley and colleagues²¹ found that 37% of patients prefer colonoscopy screening, 31% prefer FOBT, and 9% prefer sigmoidoscopy. In addition, patient preferences may vary depending on the patient subpopulation.^22-24 Therefore, it is unclear whether our finding that colonoscopy represents the dominant screening modality is a result of patient choice and is consistent with patient preferences.

Frequent use of FOBT was consistent across the 2 sites; substantial proportions of patients (between one-fourth and one-third) completed an FOBT each year. However, most patients utilizing FOBT did not use it consistently. Therefore, few patients met the criteria for screening users by having at least 3 FOBTs within the 5-year period. Among patients considered nonusers of CRC screening, more than 22% at the Michigan site and more than 43% at the New Mexico site used FOBT once or twice. Previous research demonstrated that annual adherence to FOBT is a common challenge.²⁵ We found that patients who used FOBT once or twice (but not >3 times) during the 5-year study period had a mean of almost 10 primary care visits (or 2 per year). Therefore, development of primary care clinic—based processes to ensure annual use

of testing among FOBT users, including promotion of opportunistic screening, may improve CRC screening use among insured primary care populations.

In line with previous research,^26-29 we found that the receipt of more primary care visits was associated with a greater likelihood of screening use. Nonetheless, more than one-fourth of patients who did not meet the definition of screening users had 2 or more PHEs. Although we cannot know for certain whether CRC screening was recommended by a physician during these visits, data from an observational study¹⁹ between 2007 and 2009 at the same Michigan health system as that studied herein showed that 94% of patients due for CRC screening who had a PHE received a physician recommendation for CRC screening. Such results, along with findings by others,^30,31 illustrate the necessary but insufficient role of physician recommendation in the CRC screening process and the importance of improvement in the effectiveness of provider recommendations for evidence-based care.

There are several important limitations to this study. First, we relied on automated data, which precludes our discerning whether tests were ordered for screening or diagnostic purposes or whether a colonoscopy was ordered because of another positive test result. This could overestimate screening use and confound observed differences in screening among populations if certain subgroups are more prone to the use of diagnostic vs screening tests. Second, we were limited to a 5-year observation period of continuous enrollment. Although colonoscopies performed in the 5-year period before our observation period were considered when determining screening status, patients who were not continuously enrolled during that time may have received colonoscopy screening elsewhere. Third, although the patient populations studied were large and diverse, they were all insured; while their care was delivered by 2 health systems only, we were unable to systematically evaluate institution-level factors that may have influenced screening use. Fourth, care should be taken when generalizing findings to uninsured patients, those not visiting

a primary care provider, or populations otherwise different from those studied herein. In particular, the high median annual estimated household incomes among the communities in which study patients resided should be noted. However, the national Healthcare Effectiveness Data and Information Set (HEDIS) rate for CRC screening use in commercial health plans during the same period was estimated to be about midway between our 2 observed rates (ie, 58.7%).³² Regional differences

in screening use, documented by patient self-report, indicate a similar but smaller gap between Michigan and New Mexico rates.^9,33

Among the populations studied herein, between one-third and one-half of primary care patients were not users of recommended CRC screening, and most screening users utilized colonoscopy. For patients unwilling to undergo colonoscopy, FOBT seems a viable option, but findings at both sites point to the challenges of ensuring that patients who opt for FOBT alone adhere to guidelines for repeated annual testing. Most likely to be effective are office-based processes that are able to capitalize on opportunities within the context of PHEs and other types of primary care visits. Further research is needed to determine what factors are barriers to routine FOBT or

colonoscopy use among insured patients who have access to and regularly use primary care and how those barriers can be eliminated. Given the divergent trends observed in CRC screening rates between the 2 integrated delivery systems studied herein, exploration of organizational and other contextual factors that influence CRC screening use over time in a given healthcare system may be beneficial.

Author Affiliations: From the Center for Health Services Research (DAS, JEL), Henry Ford Health System, Detroit, MI; Biostatistics and Research Epidemiology (GD), Henry Ford Health System, Detroit, MI; LCF Research (MS, MJG, DLB), Albuquerque, NM; Centers for Public Health Research and Evaluation, Battelle (DK, DEM), Seattle, WA; Division of Cancer Prevention and Control (JLS), Centers for Disease Control and Prevention, Atlanta, GA; and School of Medicine (JEL), Virginia Commonwealth University, Richmond, VA.

Funding Source: This study was supported by contract 200-2002-F-00838 from the Division of Cancer Prevention and Control, Centers for Disease Control and Prevention. The findings and conclusions in this study are those of the authors and do not necessarily represent the official views of the Centers for Disease Control and Prevention.

Author Disclosures: The authors report no relationship or financial interest with any entity that would pose a conflict of interest with the subject matter of this article.

Authorship Information: Concept and design (DAS, MJG, DK, DEM, JEL); acquisition of data (DAS, MS, DLB, JEL); analysis and interpretation of data (DAS, GD, MS, MJG, DK, DEM, JEL); drafting of the manuscript (DAS, GD, MS, MJG, DK, DEM, JEL); critical revision of the manuscript for important intellectual content (DAS, GD, MJG, DK, DEM, JLS, JEL); statistical analysis (GD); provision of study materials or patients (MS); obtaining funding (DK, DEM, JLS, JEL); administrative, technical, or logistic support (DAS, MS, JEL); and supervision (MJG, JLS, JEL).

Address correspondence to: Deirdre A. Shires, MPH, MSW, Center for Health Services Research, Henry Ford Health System, One Ford Place, Ste 3A, Detroit, MI 48202. E-mail: dshires1@hfhs.org.

1. Winawer S, Fletcher R, Rex D, et al; Gastrointestinal Consortium Panel. Colorectal cancer screening and surveillance: clinical guidelines and rationale: update based on new evidence. Gastroenterology. 2003; 124(2):544-560.

2. Ko C, Hyman NH; Standards Committee of The American Society of Colon and Rectal Surgeons. Practice parameter for the detection of colorectal neoplasms: an interim report (revised). Dis Colon Rectum. 2006;49(3):299-301.

3. Levin B, Lieberman DA, McFarland B, et al; American Cancer Society Colorectal Cancer Advisory Group, US Multi-Society Task Force, American College of Radiology Colon Cancer Committee. 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.

4. US Preventive Services Task Force. Screening for colorectal cancer: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med. 2008;149(9):627-637.

5. Rex DK, Johnson DA, Anderson JC, Schoenfeld PS, Burke CA, Inadomi JM; American College of Gastroenterology. American College of Gastroenterology guidelines for colorectal cancer screening 2009 [published correction appears in Am J Gastroenterol. 2009;104(6):1613]. Am J Gastroenterol. 2009;104(3):739-750.

6. Shapiro JA, Seeff LC, Thompson TD, Nadel MR, Klabunde CN, Vernon SW. Colorectal cancer test use from the 2005 National Health Interview Survey. Cancer Epidemiol Biomarkers Prev. 2008;17(7):1623-1630.

7. Smith RA, Cokkinides V, Brooks D, Saslow D, Brawley OW. Cancer screening in the United States, 2010: a review of current American Cancer Society guidelines and issues in cancer screening. CA Cancer J Clin. 2010;60(2):99-119.

8. Trivers KF, Shaw KM, Sabatino SA, Shapiro JA, Coates RJ. Trends in colorectal cancer screening disparities in people aged 50-64 years, 2000-2005. Am J Prev Med. 2008;35(3):185-193.

9. Rim SH, Joseph DA, Steele CB, Thompson TD, Seeff LC; Centers for Disease Control and Prevention (CDC). Colorectal cancer screening: United States, 2002, 2004, 2006, and 2008. MMWR Surveill Summ. 2011;60(suppl):42-46.

10. Christman LK, Abdulla R, Jacobsen PB, et al. Colorectal cancer screening among a sample of community health center attendees. J Health Care Poor Underserved. 2004;15(2):281-293.

11. O’Malley AS, Forrest CB, Feng S, Mandelblatt J. Disparities despite coverage: gaps in colorectal cancer screening among Medicare beneficiaries. Arch Intern Med. 2005;165(18):2129-2135.

12. Lafata JE, Williams LK, Ben-Menachem T, Moon C, Divine G. Colorectal carcinoma screening procedure use among primary care patients. Cancer. 2005;104(7):1356-1361.

13. Fenton JJ, Cai Y, Green P, Beckett LA, Franks P, Baldwin LM. Trends in colorectal cancer testing among Medicare subpopulations. Am J Prev Med. 2008;35(3):194-202.

14. Frost FJ, Tollestrup K, Trinkaus KM, et al. Mammography screening and breast cancer tumor size in female members of a managed care organization. Cancer Epidemiol Biomarkers Prev. 1998;7(7):585-589.

15. Vine MF, Degnan D, Hanchette C. Geographic information systems: their use in environmental epidemiologic research. Environ Health Perspect. 1997;105(6):598-605.

16. Deyo RA, Cherkin DC, Ciol MA. Adapting a clinical comorbidity index for use with ICD-9-CM administrative databases. J Clin Epidemiol. 1992;45(6):613-619.

17. US Preventive Services Task Force. Screening for colorectal cancer: recommendations and rationale. Ann Intern Med. 2002;137(2):129-131.

18. Klabunde CN, Lanier D, Nadel MR, McLeod C, Yuan G, Vernon SW. Colorectal cancer screening by primary care physicians: recommendations and practices, 2006-2007. Am J Prev Med. 2009;37(1):8-16.

19. McQueen A, Bartholomew LK, Greisinger AJ, et al. Behind closed doors: physician-patient discussions about colorectal cancer screening. J Gen Intern Med. 2009;24(11):1228-1235.

20. Elston-Lafata J, Cooper GS, Divine G, et al. Patient-physician discussions of colorectal cancer screening: delivery of the 5 ‘As’ in practice. Am J Prev Med. In press.

21. Hawley ST, Volk RJ, Krishnamurthy P, Jibaja-Weiss M, Vernon SW, Kneuper S. Preferences for colorectal cancer screening among racially/

ethnically diverse primary care patients. Med Care. 2008;46(9)(suppl 1):S10-S16.

22. Wolf RL, Basch CE, Brouse CH, Shmukler C, Shea S. Patient preferences and adherence to colorectal cancer screening in an urban population. Am J Public Health. 2006;96(5):809-811.

23. Marshall DA, Johnson FR, Phillips KA, Marshall JK, Thabane L, Kulin NA. Measuring patient preferences for colorectal cancer screening using a choice-format survey. Value Health. 2007;10(5):415-430.

24. Schroy PC III, Glick JT, Robinson PA, Heeren T. Screening preferences of patients at familial risk of colorectal cancer. Dig Dis Sci. 2007; 52(10):2788-2795.

25. Sonnenberg A. Cost-effectiveness in the prevention of colorectal cancer. Gastroenterol Clin North Am. 2002;31(4):1069-1091.

26. Cardarelli R, Thomas JE. Having a personal health care provider and receipt of colorectal cancer testing. Ann Fam Med. 2009;7(1):5-10.

27. Fenton JJ, Reid RJ, Baldwin LM, Elmore JG, Buist DS, Franks P. Influence of primary care use on population delivery of colorectal cancer screening. Cancer Epidemiol Biomarkers Prev. 2009;18(2):640-645.

28. Shokar NK, Carlson CA, Weller SC. Prevalence of colorectal cancer testing and screening in a multiethnic primary care population. J Community Health. 2007;32(5):311-323.

29. Zimmerman RK, Nowalk MP, Tabbarah M, Grufferman S. Predictors of colorectal cancer screening in diverse primary care practices. BMC Health Serv Res. 2006;6:e116. http://www.ncbi.nlm.nih.gov/pmc/articles/ PMC1590019/?tool=pubmed. Accessed June 20, 2011.

30. Messina CR, Lane DS, Grimson R. Colorectal cancer screening attitudes and practices preferences for decision making. Am J Prev Med. 2005;28(5):439-446.

31. Denberg TD, Melhado TV, Coombes JM, et al. Predictors of nonadherence to screening colonoscopy. J Gen Intern Med. 2005;20(11): 989-995.

32. National Committee for Quality Assurance. The State of Healthcare Quality 2009. NCQA: Washington, DC; 2009.

33. Centers for Disease Control and Prevention. Increased use of colorectal cancer tests: United States, 2002 and 2004. MMWR Morb Mortal Wkly Rep. 2006;55(11):308-311.

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