Combination of Sigmoidoscopy and a Fecal Immunochemical Test to Detect Proximal Colon Neoplasia
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1 CLINICAL GASTROENTEROLOGY AND HEPATOLOGY 2009;7: Combination of Sigmoidoscopy and a Fecal Immunochemical Test to Detect Proximal Colon Neoplasia JUN KATO,* TAMIYA MORIKAWA,* MOTOAKI KURIYAMA,* YUTAKA YAMAJI, RYOICHI WADA, TORU MITSUSHIMA, and KAZUHIDE YAMAMOTO* *Department of Gastroenterology and Hepatology, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama; Department of Gastroenterology, Graduate School of Medicine, University of Tokyo, Tokyo; and Department of Gastroenterology, Kameda General Hospital, Chiba, Japan See Editorial on page BACKGROUND & AIMS: The combination of sigmoidoscopy and a sensitive fecal occult blood test was recommended as one strategy for colorectal cancer screening by the US Preventive Services Task Force in However, there have been no studies to evaluate the sensitivity of a one-time screen that uses both flexible sigmoidoscopy and a fecal immunochemical test (FIT) to detect advanced colorectal neoplasia. METHODS: We analyzed data from 21,794 asymptomatic persons who had undergone colonoscopy and a FIT. Analyses were performed with the following assumptions: colonoscopy would be performed for any positive FIT result; colonoscopy would be performed if the FIT result was negative and if advanced neoplasia was detected in the rectosigmoid (or plus descending) colon. The sensitivities and specificities of the combination of sigmoidoscopy and the FIT in detecting advanced neoplasia in the proximal colon were determined. RESULTS: When colonoscopy was performed for a positive FIT result alone, for a positive sigmoidoscopy finding, and for a positive FIT result or sigmoidoscopy finding, the sensitivities in detection of advanced proximal neoplasia were 22.3%, 16.3%, and 31.7%, respectively. The sensitivities for detection of proximal invasive cancer were 58.3%, 8.3%, and 62.5%, respectively. CONCLUSIONS: The combination of sigmoidoscopy and FIT can detect advanced proximal neoplasia better than either test alone. The incremental yield of advanced neoplasm detection by a screening program that uses both a FIT and sigmoidoscopy is approximately 10%. The FIT adds the most in terms of finding proximal cancers in a screening program that uses both tests. The combination of sigmoidoscopy and FIT is a viable and useful screening option. Although colorectal cancer (CRC) is one of the leading causes of cancer deaths in many countries, frequently CRC patients have no associated symptoms. Therefore, CRC screening for asymptomatic adults has been recommended by a large number of organizations and expert panels. In 2008, two new guidelines for CRC screening were published in the United States. 1,2 These updated guidelines differ in specific tests recommended, but the following are recommended by one or the other of them: stool tests including the high-sensitivity guaiac fecal occult blood test (FOBT), the fecal immunochemical test (FIT), and stool DNA test, and structural examinations including flexible sigmoidoscopy, optical colonoscopy, double-contrast barium enema, and computed tomographic colonography (CTC). Optical colonoscopy has become popular as a primary screening test in recent years. Despite many studies estimating the sensitivity of colonoscopy for colorectal neoplasia 3 5 and its capability of risk reduction of developing CRC, 6 9 data are still insufficient to provide precise estimates of the sensitivity of colonoscopy in community settings. In addition, most countries do not have the monetary and manpower resources needed to provide population screening with colonoscopy, 10 and the procedure has risks for otherwise healthy people including perforation, bleeding, and reaction to drugs for conscious sedation. 11 Screening sigmoidoscopy is currently still being used in some countries. 12 Sigmoidoscopy screening, however, does not allow direct observation of neoplasia in the proximal colon. FOBT is another screening tool used in many countries, including the United Kingdom, Australia, Japan, France, Italy, Israel, and Ontario Province of Canada. In some, the highsensitivity guaiac FOBT or FIT has recently been recommended to replace the standard guaiac FOBT. 1,2 The high-sensitivity guaiac FOBT and FIT have the advantage of higher sensitivity for advanced colorectal neoplasia, although some studies have indicated that the specificity of the high-sensitivity guaiac FOBT is relatively low Another advantage of the immunochemical version is that it can be developed and read by instrument. We have already reported the sensitivity of the immunochemical test for large, clinically relevant adenomas and CRCs. 17 The performance characteristics of a strategy combining sigmoidoscopy and FOBT have been examined and reported. Some of these studies have shown increased sensitivity for advanced colorectal neoplasia, 18 and in several countries, the combined strategy has actually been adopted. 12 However, these older studies used guaiac-based traditional FOBTs. There have been no reports of a screening strategy combining sigmoidoscopy and FIT. In this study, therefore, we estimated the detectability of advanced proximal colon neoplasia achieved by combining results from sigmoidoscopy and FIT. Abbreviations used in this paper: CRC, colorectal cancer; CTC, computed tomographic colonography; FIT, fecal immunochemical test; FOBT, fecal occult blood test by the AGA Institute /09/$36.00 doi: /j.cgh
2 1342 KATO ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 7, No. 12 Methods Study Design This study consisted of an additional analysis of a cohort that we reported on previously. 17 Potentially eligible subjects were participants in a comprehensive health program at Kameda General Hospital or Kameda Makuhari Clinic between April 1983 and March We consecutively enrolled 22,666 persons who had undergone colonoscopy and FIT. All eligible subjects were asymptomatic and participated voluntarily in this program. Subjects were excluded if they reported symptoms of disease of the lower gastrointestinal tract, including visible rectal bleeding, a recent change in bowel habits, or lower abdominal pain that would normally require a medical evaluation. Information on family history with respect to CRC and the results of prior screening or diagnostic colorectal evaluations, generally, were not routinely requested or recorded. This study protocol was approved by a committee at Kameda General Hospital. Fecal Occult Blood Test We performed a 1-day, 1-sample FIT. Participants were asked to prepare a fecal sample from a stool specimen by using a collection kit (Fujirebio Inc, Tokyo, Japan). Each participant received the kit about 2 weeks before the scheduled colonoscopy. The day before colonoscopy (or on the morning of the colonoscopy), each subject collected a stool sample, making sure to keep the sample dry during collection (ie, by preventing the sample from making contact with the toilet bowl water). The stool sample was collected before the bowel preparation was begun. The participants brought the collection tubes to the hospital or clinic on the day of colonoscopy, and the samples were sent to the laboratory within 24 hours for immediate testing. We used the Magstream 1000/Hem SP automated system (Fujirebio) for the FIT. This system is based on the Immudia- Hem SP test (Fujirebio), which was the original version of HemeSelect (Beckman Coulter, Palo Alto, CA). The Magstream 1000/Hem SP system is described in detail in previous reports. 17,19 Colonoscopy On the day of colonoscopy, each subject received 2Lof a polyethylene glycol based electrolyte solution for bowel preparation, and this solution was used according to the manufacturer s instructions (Ajinomoto Pharma, Tokyo, Japan). After the colonic lavage was finished, colonoscopy was performed as described previously. 17 In all cases, the endoscopists were blinded to the results of FOBT. Complete colonoscopy was defined as insertion into the cecum, and each endoscopist was required to take pictures of the appendiceal orifice of the cecum. Subjects were excluded if the colonoscopic examination was incomplete as a result of problems with bowel preparation or failed colonoscope insertion into the cecum. During colonoscopy, the locations and sizes of all polypoid lesions were determined before their removal from the colon and recorded by endoscopists. Endoscopists used biopsy forceps as a visual guide to estimate the sizes of the polyps. Polyps measuring 4 5 mm or more in diameter were subjected to polypectomy by a diathermic snare after the completion of the study during second-look colonoscopy, whereas tissue specimens from smaller polyps were obtained with cold biopsy forceps during screening colonoscopy conducted at the time of this study. Second-look colonoscopy was required because the cost of polypectomy was not covered in this program. Pathologic Findings The methods for pathologic examination of adenomas and carcinomas were described previously. 17 Histologic characteristics of the polyps included normal mucosa, hyperplastic polyps, and adenoma. Serrated polyps except hyperplastic polyps (ie, traditional serrated adenomas or sessile serrated adenomas) were not distinguished from traditional adenomas. Hyperplastic polyps were not included as neoplasia. Advanced colonic neoplasia was defined as adenomas 10 mm or more in diameter, adenomas with high-grade dysplasia, or invasive cancer. Villous histology was not taken into consideration in determining advanced neoplasia because of the lack of such data. The locations of the neoplasia were categorized as the rectum, sigmoid colon, descending colon, transverse colon, ascending colon, and cecum. Sigmoidoscopic findings were theoretically defined as the findings in the rectosigmoid colon or the findings in the distal portion of the splenic flexure. The proximal colon indicated all proximal portions of the colon including or not including the descending colon, according to the definition of sigmoidoscopic findings. Statistical Analysis Database management and all statistical analyses were performed with SAS software (SAS Institute, Cary, NC). The sensitivity, specificity, positive, and negative were calculated on the basis of the proximal colon findings (advanced neoplasia or invasive cancer) by colonoscopy that would be performed if each screening test (sigmoidoscopy only, FIT only, or both) was positive. These s were determined with 95% confidence intervals. Theoretical sigmoidoscopic findings were analyzed in 2 different manners. In one manner, colonoscopy would be performed when advanced distal neoplasia was detected by sigmoidoscopy. The other case was that colonoscopy would be performed when any distal neoplasia was detected by sigmoidoscopy. Results Subjects Of the 22,666 persons who met the criteria for enrollment, 418 patients were excluded because of an incomplete colonoscopy (407 with failed insertion into the cecum and 11 with obstructing invasive cancer in the rectosigmoid colon). In addition, 454 patients were also excluded because of lack of sufficient information on the polypoid lesion. Thus, the data of 21,794 patients were analyzed. No serious complications were observed during or after the colonoscopy. Selected demographic characteristics of the study population are shown in Table 1. Men accounted for 72.0% of the subjects, and the mean age of all subjects was years. FIT was positive in 1220 cases (5.6%). Among the 21,794 subjects, 17,480 (80.2%) had no neoplasia. Neoplasia, as defined, was detected in 4314 subjects (19.8%); 3593 (16.5%) had adenomas 10 mm, 721 (3.3%) had advanced neoplasia, and 68 (0.3%) had invasive cancer.
3 December 2009 SIGMOIDOSCOPY PLUS FIT 1343 Table 1. Characteristics of Study Population Variable No. of patients (%) (n 21,794) Sex Male 15,684 (72.0) Female 6,110 (28.0) Age (y) Mean SD FIT 1220 (5.6) 20,574 (94.4) Finding No neoplasia 17,480 (80.2) Neoplasia 4314 (19.8) Adenomas 10 mm 3593 (16.5) Advanced neoplasia a 721 (3.3) Invasive cancer 68 (0.3) a Advanced neoplasia was defined as adenomas 10mm, adenomas with high-grade dysplasia, and invasive cancer. of Sigmoidoscopy Plus Fecal Immunochemical Test for Proximal Neoplasia The sensitivity and specificity of theoretical sigmoidoscopy plus FIT are depicted in Tables 2 5. First, analysis was performed defining sigmoidoscopic findings as the findings in the rectosigmoid colon. The sensitivities of rectosigmoid findings (advanced, rectosigmoid findings (any, and FIT for advanced proximal neoplasia were 16.3%, 37.6%, and 22.3%, respectively (Table 2). The sensitivities of the combination of theoretical sigmoidoscopy (findings of advanced neoplasia and those of any and FIT for advanced proximal neoplasia were 31.7% and 48.6%, respectively. The sensitivities of rectosigmoid findings (advanced, rectosigmoid findings (any, and FIT for proximal invasive cancer were 8.3%, 12.5%, and 58.3%, respectively (Table 3). The sensitivities of the combination of theoretical sigmoidoscopy (findings of advanced neoplasia and those of any and FIT were 62.5% and 62.5%, respectively. When the sigmoidoscopic findings were defined as the findings in the distal portion of the splenic flexure, the sensitivities of findings in the distal, findings in the distal, and FIT for advanced proximal neoplasia were 16.5%, 38.5%, and 21.5%, respectively (Table 4). The sensitivities of the combination of theoretical sigmoidoscopy (findings of advanced neoplasia and those of any and FIT were 30.0% and 48.8%, respectively. The sensitivities of findings in the distal, findings in the distal, and FIT for proximal invasive cancer were 4.3%, 8.7%, and 56.5%, respectively (Table 5). The sensitivities of the combination of theoretical sigmoidoscopy (findings of advanced neoplasia and those of any and FIT were 60.9% and 60.9%, respectively. Discussion In this study, we demonstrated the sensitivity and specificity of a one-time combined strategy with sigmoidoscopy and FIT to detect proximal colon neoplasia. Although there have been reports on performance characteristics of the combined strategy of sigmoidoscopy and FOBT, in all of these the FOBT used was the standard guaiac-based FOBT. 18,20,21 To our knowledge, there have been no such reports with the FIT. Because the immunochemical test has been replacing the standard guaiacbased test and is expected to become more prevalent, our study is relevant to CRC screening strategy in the near future. One of the recent guidelines for CRC screening recommended structural examinations such as colonoscopy, sigmoidoscopy, double-contrast barium enema, and CTC over fecal tests. 1 Another guideline made no recommendation for one kind of test over another. 2 No CRC screening test is perfect for either cancer detection or adenoma detection. Each test has unique advantages, each has been shown to be cost-effective, and each has associated limitations and risks. A principal benefit of colonoscopy is that it allows for a full structural examination of the colon and rectum in a single session. Biopsy of suspected malignancies and removal of polyps are possible as well. Nevertheless, it still has several problems such as serious complications, capacity for population screening, upfront costs, sensitivity, and effectiveness in community practice especially for right-sided advanced neoplasms. 22 The results of our study suggest that CRC screening with sigmoidoscopy and FIT is superior to screening with either Table 2. and of Rectosigmoid Findings Alone, FIT Alone, and FIT Plus Rectosigmoid for Proximal Advanced Neoplasia (%) (%) Rectosigmoid findings ( ) 98.1 ( ) 11.5 ( ) 98.7 ( ) (advanced Rectosigmoid findings ( ) 88.8 ( ) 4.8 ( ) 99.0 ( ) (any FIT ( ) 94.6 ( ) 5.8 ( ) 98.8 ( ) Rectosigmoid findings ( ) 93.3 ( ) 6.6 ( ) 98.9 ( ) (advanced or FIT Rectosigmoid findings (any ( ) 84.7 ( ) 4.5 ( ) 99.1 ( )
4 1344 KATO ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 7, No. 12 Table 3. and of Rectosigmoid Findings Alone, FIT Alone, and FIT Plus Rectosigmoid for Proximal Cancer (%) (%) Rectosigmoid findings ( ) 97.9 ( ) 0.4 ( ) 99.9 ( ) (advanced Rectosigmoid findings ( ) 88.4 ( ) 0.1 ( ) 99.9 ( ) (any FIT ( ) 94.5 ( ) 1.1 ( ) ( ) Rectosigmoid findings ( ) 93.0 ( ) 1.0 ( ) ( ) (advanced or FIT Rectosigmoid findings (any ( ) 84.2 ( ) 0.4 ( ) ( ) alone. We have previously reported that FIT could detect invasive cancer with a sensitivity of 65.8%. Thus, immunochemical testing is more sensitive than the standard guaiac-based FOBT. In addition, no dietary restriction is required. Another advantage of the immunochemical version is that it can be developed and interpreted with automation. Several reports have indicated the results of combining FOBT and sigmoidoscopy. Lieberman and Weiss 18 evaluated the performance of sigmoidoscopy by using a dataset of patients who had undergone colonoscopy, as we did here. They reported that the sensitivity of sigmoidoscopy alone and that of sigmoidoscopy plus FOBT for advanced neoplasia in the total colon were 70.3% and 75.8%, respectively. Their results and those in other previous reports 20,21 indicated that the addition of FOBT to sigmoidoscopy has little benefit for detecting advanced proximal neoplasia. All of the previous reports of a combined strategy used guaiac-based FOBT. In our study with FIT, to detect proximal invasive cancer, the sensitivity of sigmoidoscopy alone was only 12.5%, even if colonoscopy was performed in cases in which any neoplasia was found in the rectosigmoid colon. In contrast, the combined strategy increased the sensitivity to 62.5%. The addition of sigmoidoscopy to FIT increased sensitivity for advanced proximal neoplasia by nearly 10%. However, as described above, addition of sigmoidoscopy to FIT added little for detecting proximal invasive cancer. These results suggest that the combined strategy of sigmoidoscopy with FIT should be considered one of the options in one-time CRC screening to detect advanced proximal neoplasia, even if this strategy is not much superior to FIT alone for detecting proximal invasive cancer. This combined strategy can detect 48.3% of advanced neoplasia and 62.5% of invasive cancer in the proximal colon. Although the optimal screening interval is still unknown, repeated testing is necessary even for this combined strategy, as shown by computer modeling in the U.S. Preventive Services Task Force guideline. 23 There are limitations to our study. First, our study population was young (average age, 48.2 years) and male-dominant Table 4. and of the Distal Portion of the Splenic Flexure Findings Alone, FIT Alone, and FIT Plus Distal Portion of the Splenic Flexure for Proximal Advanced Neoplasia (%) (%) Findings of the distal ( ) 97.9 ( ) 8.5 ( ) 99.0 ( ) Findings of the distal ( ) 86.7 ( ) 3.4 ( ) 99.2 ( ) FIT ( ) 94.6 ( ) 4.6 ( ) 99.0 ( ) Findings of the distal ( ) 93.1 ( ) 5.0 ( ) 99.1 ( ) Findings of the distal ( ) 82.7 ( ) 3.3 ( ) 99.3 ( )
5 December 2009 SIGMOIDOSCOPY PLUS FIT 1345 Table 5. and of the Distal Portion of the Splenic Flexure Findings Alone, FIT Alone, and FIT Plus Distal Portion of the Splenic Flexure for Proximal Cancer (%) (%) Findings of the distal ( ) 97.7 ( ) 0.2 ( ) 99.9 ( ) Findings of the distal ( ) 86.4 ( ) 0.1 ( ) 99.9 ( ) FIT ( ) 94.5 ( ) 1.1 ( ) ( ) Findings of the distal ( ) 92.8 ( ) 0.9 ( ) ( ) Findings of the distal ( ) 82.4 ( ) 0.4 ( ) 99.9 ( ) (72.0%). We lacked information on family history of CRC and prior colorectal evaluations. All of the patients in this study were Japanese. The race uniformity of the study population constitutes a limitation as to applicability of our results to other ethnic populations or diverse populations. Because the cost of colonoscopy was partially paid by private company health insurance and fewer women are employed in Japan, our cohort was predominately male. Because prevalence of proximal colonic neoplasia increases with age and is higher in women than in men, 24 the results, particularly positive and negative s, for older subjects and/or for a female-dominant population would be different. Our study included many subjects who had proximal colon cancer without any neoplasia in the distal colon. This phenomenon might be attributed to the young and male-dominant population. However, few reports have indicated the prevalence of proximal neoplasia in relatively young subjects who did not have distal neoplasia. We chose a 1-day method of conducting FIT. The reason is explained in our previous report. 17 Other studies have indicated that a 2- or 3-day method is more sensitive for colorectal neoplasia. 25 Therefore, the combination of sigmoidoscopy and 2- or 3-day sampling with a FIT could be more sensitive for proximal neoplasia. We used the Magstream 1000/Hem SP system for FIT. This system is widely used in Japan and is also available in Western countries. In Japan, the OC-SENSOR (Eiken Chemical, Tokyo, Japan) is also widely used. Whereas the Magstream system has a fixed cutoff (20 ng/ml) of hemoglobin concentration, the OC-SENSOR can quantify hemoglobin concentrations up to a few ng/ml and change cutoff s to modify the sensitivity and specificity for colorectal neoplasia. Because the sensitivity for proximal advanced neoplasia was relatively low (22.3%) in our study, an increase in sensitivity by changing cutoff s might lead to a better combined strategy. Finally, the results of sigmoidoscopy in this study were theoretically derived from the results of colonoscopy. To know the real power of sigmoidoscopy, true sigmoidoscopy screening should be done. In conclusion, a combined screening strategy of sigmoidoscopy and FIT is more effective than each method alone. This strategy should be considered especially in communities that are not capable of colonoscopy screening, but it should be repeated at appropriate intervals to reduce the detection-failure rate of clinically relevant proximal lesions. References 1. Levin B, Lieberman 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: Whitlock EP, Lin JS, Liles E, et al. Screening for colorectal cancer: a targeted, updated systematic review for the U.S. Preventive Services Task Force. Ann Intern Med 2008;149: Rex DK, Rahmani EY, Haseman JH, et al. Relative sensitivity of colonoscopy and barium enema for detection of colorectal cancer in clinical practice. Gastroenterology 1997;112: Bressler B, Paszat LF, Vinden C, et al. Colonoscopic miss rates for right-sided colon cancer: a population-based analysis. Gastroenterology 2004;127: Pickhardt PJ, Nugent PA, Mysliwiec PA, et al. Location of adenomas missed by optical colonoscopy. Ann Intern Med 2004;141: Cotterchio M, Manno M, Klar N, et al. Colorectal screening is associated with reduced colorectal cancer risk: a case-control study within the population-based Ontario Familial Colorectal Cancer Registry. Cancer Causes Control 2005;16: Cress RD, Morris C, Ellison GL, et al. Secular changes in colorectal cancer incidence by subsite, stage at diagnosis, and race/ ethnicity, Cancer 2006;107: Singh H, Turner D, Xue L, et al. Risk of developing colorectal cancer following a negative colonoscopy examination: evidence for a 10-year interval between colonoscopies. JAMA 2006;295: Lakoff J, Paszat LF, Saskin R, et al. Risk of developing proximal versus distal colorectal cancer after a negative colonoscopy: a
6 1346 KATO ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 7, No. 12 population-based study. Clin Gastroenterol Hepatol 2008;6: Vijan S, Inadomi J, Hayward RA, et al. Projections of demand and capacity for colonoscopy related to increasing rates of colorectal cancer screening in the United States. Aliment Pharmacol Ther 2004;20: Gatto NM, Frucht H, Sundararajan V, et al. Risk of perforation after colonoscopy and sigmoidoscopy: a population-based study. J Natl Cancer Inst 2003;95: Benson VS, Patnick J, Davies AK, et al. Colorectal cancer screening: a comparison of 35 initiatives in 17 countries. Int J Cancer 2008;122: Allison JE, Tekawa IS, Ransom LJ, et al. A comparison of fecal occult-blood tests for colorectal-cancer screening. N Engl J Med 1996;334: St John DJ, Young GP, Alexeyeff MA, et al. Evaluation of new occult blood tests for detection of colorectal neoplasia. Gastroenterology 1993;104: Castiglione G, Zappa M, Grazzini G, et al. Immunochemical vs guaiac faecal occult blood tests in a population-based screening programme for colorectal cancer. Br J Cancer 1996;74: Allison JE, Sakoda LC, Levin TR, et al. Screening for colorectal neoplasms with new fecal occult blood tests: update on performance characteristics. J Natl Cancer Inst 2007;99: Morikawa T, Kato J, Yamaji Y, et al. A comparison of the immunochemical fecal occult blood test and total colonoscopy in the asymptomatic population. Gastroenterology 2005;129: Lieberman DA, Weiss DG. One-time screening for colorectal cancer with combined fecal occult-blood testing and examination of the distal colon. N Engl J Med 2001;345: Wong WM, Lam SK, Cheung KL, et al. Evaluation of an automated immunochemical fecal occult blood test for colorectal neoplasia detection in a Chinese population. Cancer 2003;97: Verne JECW, Aubrey R, Love SB, et al. Population based randomised study of uptake and yield of screening by flexible sigmoidoscopy compared with screening by faecal occult blood testing. BMJ 1998;317: Rasmussen M, Kronborg O, Fenger C, et al. Possible advantages and drawbacks of adding flexible sigmoidoscopy to hemoccult-ii in screening for colorectal cancer: a randomized study. Scand J Gastroenterol 1999;34: Baxter NN, Goldwasser MA, Paszat LF, et al. Association of colonoscopy and death from colorectal cancer. Ann Intern Med 2009;150: Zauber AG, Lansdorp-Vogelaar I, Knudsen AB, et al. Evaluating test strategies for colorectal cancer screening: a decision analysis for the U.S. Preventive Services Task Force. Ann Intern Med 2008;149: Nawa T, Kato J, Kawamoto H, et al. Differences between rightand left-sided colon cancer in patient characteristics, cancer morphology and histology. J Gastroenterol Hepatol 2008;23: Nakama H, Yamamoto M, Kamijo N, et al. Colonic evaluation of immunochemical fecal occult blood test for detection of colorectal neoplasia. Hepatogastroenterology 1999;46: Reprint requests Address requests for reprints to: Jun Kato, MD, Department of Gastroenterology and Hepatology, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Shikata-cho, Kita-ku, Okayama , Japan. katojun@cc. okayama-u.ac.jp; fax: (81) Conflicts of interest The authors disclose no conflicts.
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