Diagnostic Testing Following Fecal Occult Blood Screening in the Elderly

Jon D. Lurie, H. Gilbert Welch

Affiliations of authors: J. D. Lurie, Veterans Affairs Medical Center, White River Junction, VT; H. G. Welch, Veterans Affairs Medical Center, White River Junction, and Center for the Evaluative Clinical Sciences, Dartmouth Medical School, Hanover, NH.

Correspondence to present address: Jon D. Lurie, M.D., M.S., SPORT/The Spine Center, Dartmouth Hitchcock Medical Center, One Medical Center Dr., Lebanon, NH 03756-0001 (e-mail: jon.d.lurie{at}dartmouth.edu).


    ABSTRACT
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Notes
 References
 
BACKGROUND: Screening with a fecal occult blood test (FOBT) has been shown to reduce colorectal cancer mortality in controlled trials. Recently, Medicare approved payment for FOBT screening. We evaluated the pattern of diagnostic testing following the initial FOBT in elderly Medicare beneficiaries. Such follow-up testing would in the long run influence both the cost and the benefit of widespread use of FOBT. METHODS: Using Medicare's National Claims History System, we identified 24 246 Americans 65 years old or older who received FOBT at physician visits between January 1 and April 30, 1995. Prior to FOBT, these people had no evidence of any conditions for which FOBT might be used diagnostically. We examined relevant diagnostic testing in this cohort during the subsequent 8 months and determined what proportion of those received an evaluation recommended by the American College of Physicians. RESULTS: For every 1000 Medicare beneficiaries who received FOBT, 93 (95% confidence interval = 89–96 per 1000) had positive findings and relevant testing in the subsequent 8 months. Of these, 34% had the recommended evaluation of either colonoscopy or flexible sigmoidoscopy with an air-contrast barium enema. Another 34% received a partial colonic evaluation with either flexible sigmoidoscopy or a barium enema. The remaining 32% received other gastrointestinal (GI) testing without evaluation of the colonic lumen: computed tomography or magnetic resonance imaging of the abdomen (15%), upper GI series (10%), carcinoembryonic antigen (7%), and upper endoscopy (2%). Restricting the analysis to testing performed within 2 months of the initial FOBT yielded similar results. CONCLUSION: Following FOBT, many Medicare beneficiaries get further diagnostic testing, but only a small proportion receives the recommended evaluation. With this pattern of practice, population screening is likely to be more costly and less effective than estimated from controlled trials.



    INTRODUCTION
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Notes
 References
 
Screening with a fecal occult blood test (FOBT) has reduced colorectal cancer mortality by 15%–35% in randomized controlled trials (1-3). As a result, the U.S. Preventive Services Task Force (4) has endorsed annual FOBT in all persons aged 50 years or older, and Medicare (5) recently agreed to reimburse for annual screening FOBT. Despite this strong consensus supporting screening, there are many issues about specific techniques of testing and follow-up that are unresolved (6).

In the clinical trials, almost all positive FOBTs were followed-up with a complete colorectal evaluation (2,3). Typically, a single screening FOBT consists of three separate cards; the patient applies a fecal sample onto one card after each of three bowel movements and then returns the cards for processing by the laboratory. A recent clinical guideline by the American College of Physicians (7) states that any positivity on one or more cards should be followed-up with a complete colonoscopy or a flexible sigmoidoscopy with an air-contrast barium enema. Unfortunately, there is evidence that the follow-up of FOBT in the community is quite variable (3,8,9). This variation in follow-up may significantly increase the cost and decrease the effectiveness of screening and may lead some physicians to question the appropriateness of population screening (10).

In this study, we examined different diagnostic testing procedures following FOBT in elderly Medicare beneficiaries. Accurate description of current practice patterns may improve our understanding of how the efficacy of FOBT seen in clinical trials will translate into effectiveness when FOBT is used in an uncontrolled clinical environment. We attempt to shed light on the following two questions: 1) Are there additional costs that will likely accompany population screening? 2) Might the benefit of screening FOBT be lower in clinical practice than what is seen in controlled trials?


    METHODS
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Notes
 References
 
Overview

As part of work on the Dartmouth Atlas of Health Care (11), we used data from Medicare's National Claims History System to study beneficiaries who received FOBT. These files contain all physician claims for a 5% sample of Medicare Part B beneficiaries. We excluded the few beneficiaries who were younger than age 65 years and the small number enrolled in risk-contract managed care plans. Available information includes Current Procedure Terminology (CPT) codes (12); International Classification of Diseases, 9th revision (ICD-9), diagnostic codes (13); and the date of service. A detailed list of all CPT and ICD-9 codes used in these analyses appears in Appendix Table 1Go.


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Appendix Table 1. CPT* and ICD-9{dagger} codes

 
We used data from calendar year 1995. We used the first 4 months of the data to select a cohort of patients who had received FOBT. Our clinical experience has been that follow-up testing may occur over a number of months—both because patients may be slow to return their FOBT cards and because of delays in scheduling follow-up testing (sometimes reflecting system problems, sometimes patients' preferences). Therefore, we wanted to follow patients in the database as long as possible. Given the 4-month sample frame, we were able to follow each patient for a total of 8 months. To determine whether the pattern of testing was sensitive to the length of follow-up, we also repeated our analysis restricting the follow-up to 2 months.

Cohort Selection

Approximately 55 000 beneficiaries had a claim for FOBT during the first 4 months of 1995. Because FOBT is relatively inexpensive, it may be performed more often than it is billed for. As a result, the 55 000 beneficiaries whom we identified may only be a subset of the Medicare population who received FOBT.

Medicare only recently approved payment for screening FOBT; therefore, there was no direct way to separate screening FOBTs from those obtained as part of a specific diagnostic work-up. However, we defined a cohort whom we believe represents a screening population, generally defined as a population that lacks any clinical evidence of the target condition. We excluded beneficiaries with claims-based evidence of conditions for which FOBT might be used diagnostically. Specific exclusion criteria included ICD-9 codes for any of the following: digestive system disease; general symptoms, such as anorexia, weight loss, or abdominal pain; anemia; or any neoplasm. Additional exclusion criteria included CPT codes for diagnostic tests, such as iron studies, bone marrow examination, liver function tests, or abdominal radiographs. Beneficiaries were excluded if any of these codes appeared in the 1995 claims data prior to or on the same day as the initial FOBT. The final study cohort included 24 246 people.

Definition of a Positive Screen

Although we do not know which FOBTs were positive, we used as a proxy measure those FOBTs that were followed by relevant diagnostic testing. Those beneficiaries who had a positive FOBT that was not acted upon would be missed by this definition. Those who had relevant testing for unrelated reasons would be falsely included.

Relevant Downstream Events

We followed each beneficiary in the cohort for 8 months after their initial FOBT and assessed the following three major categories of subsequent diagnostic testing: 1) complete colonic evaluation—colonoscopy or flexible sigmoidoscopy with air-contrast barium enema; 2) partial colonic evaluation—flexible sigmoidoscopy alone, flexible sigmoidoscopy with single column barium enema, or a barium enema only; and 3) other gastrointestinal (GI) testing—computed tomography or magnetic resonance imaging of the abdomen, upper GI series, serum carcinoembryonic antigen levels, or esophagogastroduodenoscopy.

One possible diagnostic follow-up for a positive FOBT is to repeat the FOBT (6). However, there are other reasons to repeat a FOBT, such as the specimen was inadequate, only one of the three cards was completed, or the specimen was placed on the wrong side of the card. As a result, we do not believe that repeat FOBT is a reliable indicator of an initial positive FOBT in the Medicare claims data and did not include it as part of our relevant downstream events.

Statistical Methods

We calculated 95% confidence intervals (CIs) by using the exact binomial CI function for proportions in StataTM Software (Stata Statistical Software, release 5.0, 1997; published by Stata Corp., College Station, TX).

To help confirm the validity of our cohort as a screening cohort, we estimated the positive predictive value of FOBT in the subset of patients receiving a subsequent complete colonic evaluation. We used this subgroup because these patients are the only ones in whom the presence of cancer or polyps (the numerator) can be reliably determined. Those people who did not receive a complete evaluation may have had colorectal cancer or polyps that remained undiagnosed during the study period.

We defined the positive predictive value as the proportion of beneficiaries with an FOBT followed by a complete colonic evaluation who had either colorectal cancer or polyps. To calculate the number of patients with disease (the numerator of the positive predictive value), we developed claims-based definitions for new cases of colorectal cancer and colon polyps. Colorectal cancer was defined as an ICD-9 code for any malignant neoplasm of the GI tract, including carcinoma in situ, which was accompanied by a CPT code for treatment: colonic surgery, endoscopic excision or fulguration, radiation therapy, or chemotherapy. The presence of polyps was defined by a CPT code indicating endoscopy with polypectomy. The denominator of the positive predictive value was all beneficiaries with a complete colonic evaluation (i.e., colonoscopy or flexible sigmoidoscopy plus an air-contrast barium enema) following their initial FOBT.


    RESULTS
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 Abstract
 Introduction
 Methods
 Results
 Discussion
 Notes
 References
 
Overall, 93 people for every 1000 screened (2245 of the cohort of 24 246) received relevant subsequent diagnostic testing corresponding to an estimated positivity rate of 9.3%. The proportion with a positive screen was similar in those aged 65–74 years and those aged 75 years or more—9.3% and 9.1% respectively.

Table 1Go shows our primary findings: the numbers of people undergoing various diagnostic tests per 1000 following FOBT. All results are rounded to the nearest whole number per 1000. The proportion of all subsequent testing that occurred in each category of follow-up testing is reported to the nearest whole percent; raw counts are available in Appendix Table 2Go. Approximately 32 (95% CI = 30-34 per 1000) people underwent the recommended evaluation for every 1000 receiving an initial FOBT; however, this group represents only 34% of those undergoing subsequent diagnostic testing. Almost as many people received a partial colonic evaluation (31 per 1000; 95% CI = 29-34 per 1000) or one of the "other GI" tests without evaluation of the colonic lumen (29 per 1000; 95% CI = 27-32 per 1000).


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Table 1. Diagnostic testing in the 8-month period following initial screening with fecal occult blood test in Medicare beneficiaries*

 

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Appendix Table 2. Raw counts of beneficiaries receiving the initial fecal occult blood test and the follow-up testing

 
Not shown in Table 1Go is the proportion of people who received multiple diagnostic procedures. Among those receiving the recommended complete colonic evaluation, 28% underwent additional diagnostic testing—17% received additional evaluation of the upper GI tract and 14% received abdominal computed tomography or magnetic resonance imaging. Among those receiving a partial colonic evaluation, 13% also received upper GI tract testing.

In Fig. 1,Go we compare the results at 2 and 8 months following the initial FOBT to determine whether the pattern of testing was sensitive to the length of follow-up. Approximately half of all subsequent testing occurred within 2 months of the initial FOBT. The pattern of testing at 2 months was similar to that at 8 months. Among beneficiaries receiving subsequent testing within 2 months, 30% (95% CI = 27%–32%) received the recommended evaluation compared with 34% (95% CI = 33%–36%) at 8 months, 40% (95% CI = 37%–43%) received only a partial colonic evaluation compared with 34% (95% CI = 32%–36%) at 8 months, and 30% (95% CI = 27%–33%) received other GI testing without an evaluation of the colonic lumen compared with 32% (95% CI = 30%–34%) at 8 months. Overall, the pattern of testing was not very sensitive to the length of follow-up.



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Fig. 1. Proportion (95% confidence intervals) of Medicare beneficiaries receiving diagnostic testing within 2 months and 8 months following the initial fecal occult blood testing (FOBT). Categories of follow-up testing: {block} = complete colonic; = partial colonic; {square} = other gastrointestinal testing.

 
In Fig. 2,Go we compare subsequent diagnostic testing for those beneficiaries of ages 65-74 years and those beneficiaries of ages 75 years and older. The proportion of beneficiaries with subsequent testing who received a complete colonic evaluation was similar in both groups, 33% (95% CI = 30%–37%) for those 75 years old or older compared with 35% (95% CI = 33%–38%) for those 65–74 years old. The older beneficiaries were slightly less likely to receive a partial colonic evaluation, 30% (95% CI = 27%–33%) compared with 36% (95% CI = 34%–39%) for the younger beneficiaries. Moreover, the older beneficiaries were slightly more likely to receive other GI testing, 37% (95% CI = 33%-40%) compared with 29% (95% CI = 26%-31%) for the younger group.



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Fig. 2. Proportion (95% confidence intervals) of Medicare beneficiaries in two age groups receiving different categories of diagnostic testing following the initial fecal occult blood testing. GI = gastrointestinal. Categories of follow-up testing: {block} = complete colonic; = partial colonic; {square} = other GI testing.

 
Table 2Go shows the number of patients with colon cancer or colon polyps in the group receiving the recommended evaluation. Of the 774 beneficiaries who received a complete colonic evaluation following their FOBT, 241 had colon polyps, resulting in a positive predictive value for polyps of 0.31 (95% CI = 0.28–0.35). Of these same 774 beneficiaries, 32 had colon cancer, resulting in a positive predictive value for cancer of 0.04 (95% CI = 0.03-0.06).


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Table 2. Number of people with disease and predictive value of a positive fecal occult blood test among Medicare beneficiaries receiving the recommended complete colonic evaluation*

 

    DISCUSSION
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 Abstract
 Introduction
 Methods
 Results
 Discussion
 Notes
 References
 
Among Medicare beneficiaries who had an FOBT in the absence of apparent GI disease, about 9.3% received subsequent diagnostic testing, of whom only about a third received a complete colonic evaluation. Such a low rate of recommended follow-up would reduce the effectiveness of population screening. In addition, many people received multiple tests, which would increase the costs of population screening. With the use of Medicare's relative value scale (a low estimate of actual expenditures), the estimated cost of subsequent diagnostic testing would be more than $42 000 for every 1000 screened. Of this total cost, $23 000 would be spent on the recommended follow-up testing, while $19 000 would go to other tests. These other diagnostic evaluations add costs to population screening (an additional $6000 per cancer case detected) that would be overlooked if one examined only clinical trial data.

We found an estimated positivity rate of 9.3%. It is quite possible that the real positivity rate in our cohort was higher but that some people received no follow-up testing at all. To the degree that this undercounting of a positive screen occurred, the proportion of people with a positive FOBT who received the recommended evaluation would be even lower than the 34% that we observed. Alternatively, the actual positivity rate may have been lower than 9.3%, and we may have overcounted by including unrelated follow-up testing. However, 9.3% is about what we would predict for a positivity rate in this cohort. The expected positivity rate is 2%–4% with nonrehydrated slides and 8%–16% with rehydrated slides (6). The positivity rate in our cohort should be at the high end of this range because the rate of FOBT positivity increases with age (3,14,15) and our entire cohort was 65 years old or older, with 40% older than age 75 years. However, even if we drastically overcounted and the actual positivity rate were only about 4%, there still would have been only three quarters of the beneficiaries who received the recommended follow-up.

Our findings of a low rate of recommended follow-up are consistent with previous data on the work-up of positive FOBT in the community. Table 3Go summarizes some literature and puts our results in context. In randomized trials, the proportion of people with a positive FOBT who received the recommended follow-up was as high as 90% (2). In the community setting, however, the proportion with the recommended follow-up has been as low as 21% (8).


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Table 3. Range of results in the literature on recommended follow-up testing after initial fecal occult blood test

 
There are several limitations to claims data analysis in this setting. We do not know if we truly studied a screening cohort. If the FOBTs were obtained to diagnose specific symptoms or conditions, then it would be difficult to draw conclusions about the appropriateness of the follow-up testing without knowing specific clinical details. Although we used strict criteria for excluding patients with any evidence of a condition for which FOBT might be used diagnostically, diagnostic data could be missing. Nevertheless, there are two reasons why we are confident that we studied a screening cohort. First, the incidence of colon cancer in our cohort (about three per 1000 per year) and the positive predictive value of FOBT were similar to those found in screening trials (3,6). With respect to colon cancer risk and case patients detected, our cohort resembles a screening cohort. Second, we examined an additional, more narrowly defined, cohort and found almost identical results. The alternative cohort (n = 8486) was defined as patients with a specific ICD-9 code for "general medical examination," "general laboratory examination," "special screening for malignant neoplasm," or "multiphasic screening" on the day of their FOBT. Of those receiving subsequent testing in this alternative cohort, 34% received the recommended evaluation, 31% received only a partial colonic evaluation, and 35% received other GI testing.

A second limitation to our analysis is that we do not know the results of the FOBT or whether the subsequent testing was directly related to those results. Some of the subsequent testing could represent background testing unrelated to the FOBT or related to new conditions that emerged after the initial FOBT. Our exclusion criteria should have eliminated those beneficiaries with other clinical reasons for receiving the subsequent diagnostic tests that we studied. Of course, our exclusion criteria may have missed some patients with gastrointestinal problems. However, we are confident that the subsequent testing was related to the initial FOBT for two reasons. First, our finding that 9.3% of beneficiaries underwent subsequent diagnostic testing is consistent with the expected positivity rate and supports the hypothesis that we measured true follow-up testing. Second, the time course of subsequent testing, with half of all subsequent tests occurring in the first 2 months after the initial FOBT, strongly suggests a link between the subsequent testing and the initial FOBT. It is unlikely that new conditions arose after the initial FOBT to prompt testing in this short time frame.

Despite our efforts to confirm the validity of our findings, the reader might take the "other" diagnostic testing (computed tomography, magnetic resonance imaging, or carcinoembryonic antigen) as prima facie evidence that these tests were not done as part of screening for colorectal cancer. However, it is worth considering that this other testing may in fact represent real world practice. FOBT is relatively cheap, easy, and noninvasive; therefore, it may be ordered without much thought to follow-up. In fact, Cooper et al. (16) found that almost a third of primary care physicians surveyed would recommend FOBT even for a 75-year-old patient with unresectable non-small-cell lung cancer. However, when faced with a positive test and the prospect of an invasive follow-up test like colonoscopy, the physician or patient might reconsider. In the same study by Cooper et al. (16), physicians were often reluctant to recommend sigmoidoscopy even when it would have been appropriate. Thus, if FOBT were performed on some Medicare beneficiaries for whom physicians were reluctant to pursue endoscopy, these other tests might have been obtained as less invasive substitutes to follow-up on positive screens. This hypothesis is supported by the finding that these other GI tests were performed slightly more often on the older beneficiaries than on the younger ones. The low proportion of patients receiving the recommended evaluation may then represent a combination of incomplete follow-up in some case patients and a reconsideration of the initial screening decision in others.

Implications

We found a substantial amount of testing other than colon evaluations that occurred following FOBT. Some people might argue that this other testing is not extraneous but rather is indicated. In particular, Hsia et al. (17) showed that important upper GI tract lesions were common in patients with a positive FOBT. Similarly, a recent study (18) identified upper tract lesions as the cause of positive FOBT more often than colon lesions. Nearly 60% of these upper GI tract lesions resulted in a change in the patient's treatment. Thus, while upper GI tract evaluation is certainly ineffective for detecting colon cancer, it is not surprising that many physicians might pursue such testing after a positive FOBT. However, these additional tests represent substantial additional costs to screening that are largely ignored in formal cost-effectiveness models (19). Furthermore, including upper GI tract evaluation in the diagnostic follow-up of positive screening FOBT amounts to screening for upper GI tract lesions. Although these tests may detect important lesions, there is no evidence that screening for these lesions is beneficial. There is an important need to better define which follow-up diagnostic procedures are truly useful following screening FOBT.

Fueled by the knowledge of benefit from FOBT screening in clinical trials, there is almost unanimous endorsement of colorectal cancer screening with FOBT. However, screening FOBT is a complex task, and myriad clinical details will determine the effectiveness of population screening. The screening FOBT offers little benefit without proper follow-up testing and treatment. Thus, the effectiveness of screening will be reduced if only a small proportion of people receives the recommended follow-up evaluation. Our study suggests that, with current patterns of practice, population screening may be less effective than estimated from controlled trials.

We cannot determine from this study why only about a third of Medicare beneficiaries received the recommended follow-up testing. It may be that physicians were hesitant to recommend invasive testing in some patients and sought less invasive alternative follow-up tests. It may be that patients were hesitant to follow the physicians' recommendation for a complete colonic evaluation. It is important to note that, while our data were from 1995, the American College of Physician's guideline for colorectal cancer screening (7) was not published until 1997. Current physician practice may adhere more closely to the recommended complete colonic evaluation as consensus on the proper approach to colorectal cancer screening evolves. Further evaluation of current practice patterns following screening FOBT should help answer this question. Future work should focus on evaluating the usefulness of different follow-up tests after a positive FOBT, why physicians choose different follow-up tests after their patient has a positive FOBT, and patients' understanding of the downstream consequences of FOBT when they decide whether or not to be screened.


    NOTES
 
We are indebted to Chiang-Hua Chang for her expert analytic support and her incredible patience. We also thank Drs. Steven Woloshin and Steve Bensen and our two anonymous reviewers for their helpful critiques of this manuscript.


    REFERENCES
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Notes
 References
 

1 Hardcastle JD, Chamberlain JO, Robinson MH, Moss SM, Amar SS, Balfour TW. Randomised controlled trial of faecal-occult-blood screening for colorectal cancer. Lancet 1996;348:1472-7.[Medline]

2 Kronborg O, Fenger C, Olsen J, Jorgensen OD, Sondergaard O. Randomised study of screening for colorectal cancer with faecal-occult-blood test. Lancet 1996;348:1467-71.[Medline]

3 Mandel JS, Bond JH, Church TR, Snover DC, Bradley GM, Schuman LM, et al. Reducing mortality from colorectal cancer by screening for fecal occult blood. Minnesota Colon Cancer Control Study [published erratum appears in N Engl J Med 1993;329:672]. N Engl J Med 1993;328:1365-71.[Abstract/Free Full Text]

4 U.S. Preventive Services Task Force. Guide to clinical preventive services. 2nd ed. Baltimore (MD): Williams & Wilkins; 1996.

5 1998 Medicare Prevention Benefits. Available from: URL: http://www.hcfa.gov/medicare/prevent/physhelp.htm

6 Ransohoff DF, Lang CA. Screening for colorectal cancer with the fecal occult blood test: a background paper. American College of Physicians. Ann Intern Med 1997;126:811-22.[Abstract/Free Full Text]

7 American College of Physicians. Suggested technique for fecal occult blood testing and interpretation in colorectal cancer screening. A position paper.Ann Intern Med 1997;126:808-10.[Free Full Text]

8 Klos SE, Drinka P, Goodwin JS. The utilization of fecal occult blood testing in the institutionalized elderly. J Am Geriatr Soc 1991;39: 1169-73.[Medline]

9 Myers RE, Balshem AM, Wolf TA, Ross EA, Millner L. Screening for colorectal neoplasia: physicians' adherence to complete diagnostic evaluation. Am J Public Health 1993;83:1620-2.[Abstract]

10 Simon JB. Should all people over the age of 50 have regular fecal occult-blood tests? Postpone population screening until problems are solved. N Engl J Med 1998;338:1151-2; discussion 1154-5.[Free Full Text]

11 Wennberg J, Cooper M, editors. The Dartmouth atlas of health care 1998. Hanover (NH): American Hospital Publishing, Inc.; 1998.

12 American Medical Association. Physicians' Current Procedural Terminology: CPT. Chicago (IL): American Medical Association; 1994.

13 Health Care Financing Administration. International Classification of Diseases, 9th revision, clinical modification. Washington (DC): Public Health Service, U.S. Dept. of Health and Human Services; 1995.

14 Ahlquist DA, Wieand HS, Moertel CG, McGill DB, Loprinzi CL, O'Connell MJ, et al. Accuracy of fecal occult blood screening for colorectal neoplasia. A prospective study using Hemoccult and HemoQuant tests. JAMA 1993;269:1262-7.[Abstract]

15 Allison JE, Tekawa IS, Ransom LJ, Adrain AL. A comparison of fecal occult-blood tests for colorectal-cancer screening. N Engl J Med 1996;334:155-9.[Abstract/Free Full Text]

16 Cooper GS, Fortinsky RH, Hapke R, Landefeld S. Primary care physician recommendations for colorectal cancer screening: patient and practitioner factors. Arch Intern Med 1997;157:1946-50.[Abstract]

17 Hsia PC, al-Kawas FH. Yield of upper endoscopy in the evaluation of asymptomatic patients with Hemoccult-positive stool after a negative colonoscopy. Am J Gastroenterol 1992;87:1571-4.[Medline]

18 Rockey DC, Koch J, Cello JP, Sanders LL, McQuaid K. Relative frequency of upper gastrointestinal and colonic lesions in patients with positive fecal occult-blood tests. N Engl J Med 1998;3390:153-9.

19 Wagner JL, Herdman RC, Wadhwa S. Cost effectiveness of colorectal cancer screening in the elderly. Ann Intern Med 1991;115:807-17.[Medline]

20 Morris JB, Stellato TA, Guy BB, Gordon NH, Berger NA. A critical analysis of the largest reported mass fecal occult blood screening program in the United States. Am J Surg 1991;161:101-5; discussion 105-6.[Medline]

21 Levin B, Hess K, Johnson C. Screening for colorectal cancer. A comparison of 3 fecal occult blood tests. Arch Intern Med 1997;157:970-6.[Abstract]

Manuscript received March 30, 1999; revised July 20, 1999; accepted August 6, 1999.


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