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16. 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 Jun;104(6):1613]. Am J Gastroenterol. 2009;104(3): 739-750. 17. Maxwell AE, Crespi CM, Antonio CM, Lu P. Explaining disparities in colorectal cancer screening among five Asian ethnic groups: a population-based study in California. BMC Cancer. May 19 2010;10:214. 18. Doubeni CA, Laiyemo AO, Klabunde CN, Young AC, Field TS, Fletcher RH. Racial and ethnic trends of colorectal cancer screening among Medicare enrollees. Am J Prev Med. 2010;38(2):184-191. 19. Vijan S, Hwang EW, Hofer TP, Hayward RA. Which colon cancer screening test? a comparison of costs, effectiveness, and compliance. Am J Med. 2001;111 (8):593-601. 20. Heisler M, Cole I, Weir D, Kerr EA, Hayward RA. Does physician communication influence older patients’ diabetes self-management and glycemic control? results from the Health and Retirement Study (HRS). J Gerontol A Biol Sci Med Sci. 2007;62(12):1435-1442. 21. Stewart MA. Effective physician-patient communication and health outcomes: a review. CMAJ. 1995;152(9):1423-1433. 22. Anderson CJ. The psychology of doing nothing: forms of decision avoidance result from reason and emotion. Psychol Bull. 2003;129(1):139-167. 23. Redelmeier DA, Shafir E. Medical decision making in situations that offer multiple alternatives. JAMA. 1995;273(4):302-305. 24. Jones RM, Vernon SW, Woolf SH. Is discussion of colorectal cancer screening

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options associated with heightened patient confusion? Cancer Epidemiol Biomarkers Prev. 2010;19(11):2821-2825. Inadomi JM, Kuhn L, Vijan S, Fendrick AM, McMahon LF, Hayward RA. Adherence to competing colorectal cancer screening strategies. Am J Gastroenterol. 2005;100:S387-S388. Segnan N, Senore C, Andreoni B, et al; SCORE2 Working Group-Italy. Randomized trial of different screening strategies for colorectal cancer: patient response and detection rates. J Natl Cancer Inst. 2005;97(5):347-357. Segnan N, Senore C, Andreoni B, et al; SCORE3 Working Group-Italy. Comparing attendance and detection rate of colonoscopy with sigmoidoscopy and FIT for colorectal cancer screening. Gastroenterology. 2007;132(7):2304-2312. Ioannou GN, Chapko MK, Dominitz JA. Predictors of colorectal cancer screening participation in the United States. Am J Gastroenterol. 2003;98(9):20822091. Seeff LC, Nadel MR, Klabunde CN, et al. Patterns and predictors of colorectal cancer test use in the adult US population. Cancer. 2004;100(10):2093-2103. 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. Franzini L, Ribble JC, Keddie AM. Understanding the Hispanic paradox. Ethn Dis. 2001;11(3):496-518. Schwartz B. The Paradox of Choice: Why More Is Less. New York, NY: Ecco; 2004. Iyengar S. The Art of Choosing. New York, NY: Twelve; 2010.

INVITED COMMENTARY

The Importance of Choosing Colorectal Cancer Screening Tests When people have no choice, life is almost unbearable. . . . But as the number of choices keeps growing . . . choice no longer liberates, but debilitates. Barry Schwartz1(p2)

Colorectal cancer (CRC) incidence and mortality is decreasing in the United States, owing in large part to increased uptake of CRC screening.2 The incidence of CRC has decreased from 59.5 per 100 000 population in 1975 to 44.7 per 100 000 in 2007, and the CRC death rate has decreased from 28.6 per 100 000 population in 1976 to 16.7 per 100 000 in 2007.3 Not everyone is benefiting equally from this decline, however. In a recent American Cancer Society analysis, the decrease in CRCrelated death rates between 1990 and 1994 and between 2003 and 2007 ranged from 9% in Alabama to greater than 33% in Massachusetts, Rhode Island, New York, and Alaska, but Mississippi and Wyoming showed no significant decrease. There is clearly a strong imperative to continue all efforts to increase screening rates. If screening uptake can be increased, we can expect substantial continued declines in CRC incidence and mortality.2 The potential barriers to CRC screening are numerous and include fear of invasive tests, aversion to the bowel preparation, and lack of insurance coverage or access to care. Focus groups have identified other barriers, such as “parasexual” sensitivities related to homophobia or prior sexual trauma, fatalism, negative past experiences with testing, and skepticism about the financial motivation behind screening recommendations.4 These barriers may be surmountable through effective physician-

patient communication, and a physician’s recommendation is pivotal to whether patients get screened for CRC.5 What should physicians recommend when talking with patients about CRC? The psychology literature has noted that too much choice is a problem in current society.1 Patients may be overwhelmed by the options and feel that no option is perfect and therefore choose to do nothing out of confusion.6 However, every option for CRC screening has its own unique strengths and limitations. A patientcentered approach would take each patient’s perspective into account when designing a screening strategy. To test this empirically, Inadomi and colleagues7 undertook a quasiexperimental trial in the racially and ethnically diverse public health care system in San Francisco, California. They used clinic time block as the unit of randomization and every 3 months randomly allocated primary care providers (PCPs) to a different initial screening recommendation: fecal occult blood testing (FOBT), colonoscopy, or a choice between the two. A strength of this study was that participants only received credit for completing the FOBT strategy if they completed a colonoscopy if the test result was positive. Of the 997 participants enrolled, 58% completed the CRC screening strategy they were assigned or chose. Patients who were recommended colonoscopy completed screening nearly half as often (38%) as participants who were recommended FOBT (67%) (P⬍ .001) or a choice between FOBT or colonoscopy (69%) (P⬍ .001). Latinos and Asians (who were primarily Chinese) com-

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pleted screening more often than African Americans. White participants adhered more often to colonoscopy, while participants of other races or ethnicities preferred FOBT. The PCPs in this study also played an important role. As a result of participating, they were probably better informed and more likely to recommend CRC screening than the average paper chart-based or electronic reminder systems. They were blinded, however, to the screening strategy until the first day that a rotation in block occurred. An important implication of this research is that the notion of “preferred” CRC screening test should include both the physician’s and the patient’s perspective. From a gastroenterologists perspective, it may seem that colonoscopy is the preferred CRC screening strategy.8 As shown in the study by Inadomi et al,7 a recommendation for colonoscopy only would result in substantially fewer overall patients being screened and fewer cancers and advanced adenomas being detected. Many patients prefer to have a stool testing option, and including that option results in more patients being screened. The patient perspective on screening varies with race and ethnicity, which may be related to health beliefs, socioeconomic status, or language. As shown in the US Preventive Services Task Force–sponsored cost-effectiveness analysis, when colonoscopy and highly sensitive FOBT both have 100% adherence, similar life years are gained from screening with either test.9 The study by Inadomi et al7 prompts several questions for further research. Are these results applicable to other settings with other patients and PCPs? Was there something unique about these patients that made FOBT a more attractive screening option for them? Although not stated in the article, the test used in this study was most likely a standard sensitivity guaiac FOBT. Many screening programs are now using fecal immunochemical tests (FITs), since they have higher sensitivity, with preserved specificity, and require fewer specimens compared with guaiac FOBT.10 Would the use of FITs have led to an even higher participation advantage for fecal screening compared with colonoscopy? Since fecal tests need to be performed annually, can the participation advantage for fecal screening be sustained over attempts at serial screening? Can strategies be developed to increase adherence with follow-up colonoscopy after a positive FOBT or FIT result? Finally, organized screening programs frequently use mailed outreach to deliver CRC screening invitations to all members of the population

who are due for screening.10 Is the participation advantage for fecal screening preserved (or even increased) when the screening invitation is delivered by mail? If having too many choices leads to confusion, the study by Inadomi et al7 demonstrates that not having enough choice may lead to inaction when the only choice is colonoscopy. This study also shows that well-informed PCPs, focused on CRC screening, can have a meaningful impact on their patients’ adherence with screening. When it comes to CRC screening, providing an option other than colonoscopy for our patients is not overwhelming, but necessary. Theodore R. Levin, MD Author Affiliation: Department of Gastroenterology, Kaiser Permanente Medical Center, Walnut Creek, California. Correspondence: Dr Levin, Department of Gastroenterology, Kaiser Permanente Medical Center, 1425 S Main St, Walnut Creek, CA 94596 (theodore.levin@kp.org). Financial Disclosure: None reported. Funding/Support: This Invited Commentary was partly funded by grant 5U54CA163262-02 from the National Cancer Institute. 1. Schwartz B. The Paradox of Choice. New York, NY: Harper Collins; 2004. 2. Edwards BK, Ward E, Kohler BA, et al. Annual report to the nation on the status of cancer, 1975-2006, featuring colorectal cancer trends and impact of interventions (risk factors, screening, and treatment) to reduce future rates. Cancer. 2010;116(3):544-573. 3. Richardson LC, Tai E, Rim SH, Joseph D, Plescia M; Centers for Disease Control and Prevention (CDC). Vital signs: Colorectal cancer screening, incidence, and mortality—United States, 2002-2010. MMWR Morb Mortal Wkly Rep. 2011;60(26):884-889. 4. Jones RM, Devers KJ, Kuzel AJ, Woolf SH. Patient-reported barriers to colorectal cancer screening: a mixed-methods analysis. Am J Prev Med. 2010; 38(5):508-516. 5. Zapka JM, Klabunde CN, Arora NK, Yuan G, Smith JL, Kobrin SC. Physicians’ colorectal cancer screening discussion and recommendation patterns. Cancer Epidemiol Biomarkers Prev. 2011;20(3):509-521. 6. Jones RM, Vernon SW, Woolf SH. Is discussion of colorectal cancer screening options associated with heightened patient confusion? Cancer Epidemiol Biomarkers Prev. 2010;19(11):2821-2825. 7. Inadomi JM, Vijan S, Janz NK, et al. Adherence to colorectal cancer screening: a randomized clinical trial of competing strategies. Arch Intern Med. 2012; 172(7):575-582. 8. 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 [corrected]. Am J Gastroenterol. 2009;104(3):739-750. 9. Zauber AG, Lansdorp-Vogelaar I, Knudsen AB, Wilschut J, van Ballegooijen M, Kuntz KM. Evaluating test strategies for colorectal cancer screening: a decision analysis for the US Preventive Services Task Force. Ann Intern Med. 2008;149(9):659-669. 10. Levin TR, Jamieson L, Burley DA, Reyes J, Oehrli M, Caldwell C. Organized colorectal cancer screening in integrated health care systems. Epidemiol Rev. 2011;33(1):101-110.

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The Importance of Choosing Colorectal Cancer Screening Tests