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(Radiology. 2000;215:327-335.)
© RSNA, 2000

Special Review

Screening for Colorectal Cancer1

G. Scott Gazelle, MD, MPH, PhD, Pamela M. McMahon, BS and Francis J. Scholz, MD

1 From the Department of Radiology, Decision Analysis and Technology Assessment Group, Zero Emerson Pl, Suite 2H, Boston, MA 02114 (G.S.G., P.M.M.) and the Lahey Clinic Foundation, Burlington, Mass (F.J.S.). Received July 1, 1999; revision requested August 9; revision received October 11; accepted November 18. Address correspondance to G.S.G. (e-mail: gazelle@nmr.mgh.harvard.edu).

Abstract

Colorectal cancer is the third most commonly diagnosed cancer and the second leading cause of cancer deaths in the United States. Fortunately, both the incidence and mortality associated with the disease have declined during the past 2 decades. This is likely due, at least in part, to improved efforts at screening and more aggressive removal of adenomatous polyps. However, colorectal cancer screening is still generally underutilized. This article reviews the current status and future outlook for colorectal cancer screening, including a discussion of risk factors for the disease, its anatomic distribution, proposed mechanisms of development from adenomatous polyps, rationale for screening, and screening options. Published literature concerning the cost-effectiveness of colorectal cancer screening is also summarized. The article concludes with a discussion of the emerging consensus regarding the importance of and approaches to screening.

Index terms: Barium enema examination, 75.128 • Cancer screening, 75.128, 75.129, 75.321 • Colon, neoplasms, 75.128, 75.129, 75.321 • Colonoscopy, 75.129 • Cost-effectiveness • Review

There is now substantial evidence that reductions in colorectal cancer mortality can be achieved through detection and treatment of early-stage cancers (1–6). We review several factors related to the development and detection of colorectal cancer, including: (a) the key statistics, (b) the risk factors for colorectal cancer, (c) the anatomic distribution of colorectal cancer, and (d) the adenoma-carcinoma sequence. We discuss the rationale and options for colorectal cancer screening and summarize the findings of several published cost-effectiveness analyses of colorectal cancer screening. We conclude with a discussion of the emerging consensus regarding colorectal cancer screening and the important role that radiologists can play.

KEY STATISTICS

Colorectal cancer ranks as the third most commonly diagnosed cancer and the second leading cause of cancer deaths in the United States (7). The American Cancer Society (7) estimates that approximately 130,000 new cases of colorectal cancer were diagnosed in the United States in 1999 and approximately 57,000 Americans died of the disease. Colorectal cancer thus represents approximately 11% of all new cases of cancer. The lifetime risk of developing colorectal cancer has been estimated at approximately 6%, while the estimated lifetime risk of colorectal cancer death is approximately 2.6% (7). It has been estimated that a patient dying of colorectal cancer loses 13 years of life on average. Colorectal cancer affects men and women with nearly equal frequency and is the third most common cancer in both men (after lung and prostate cancer) and women (after lung and breast cancer) (7).

Survival of patients with colorectal cancer depends to a large extent on the stage of disease at diagnosis. Thus, in patients with localized disease, 5-year survival is approximately 90%, whereas in patients with regional spread of disease, 5-year survival decreases to approximately 60%. In patients with distant metastases, 5-year survival is less than 10% (7). Unfortunately, only a minority of colorectal cancers are discovered when they are still localized (7).

Both the incidence and mortality associated with colorectal cancer have declined substantially during the past 2 decades. For example, between 1973 and 1995, the incidence of colorectal cancer declined by more than 7%, while the disease-related mortality declined by almost 21% (8). These improvements may have been due to increased screening and more aggressive removal of adenomatous polyps, as well as improvements in therapy for the disease and its complications. Nevertheless, and despite increasing evidence that supports the benefits of colorectal cancer screening, the appropriateness of the different screening strategies is uncertain, and compliance with existing screening recommendations is poor (9).

RISK FACTORS FOR COLORECTAL CANCER

Several potential risk factors for the development of colorectal cancer have been identified. However, it is important to note that approximately 75% of colorectal cancers occur in patients with no known predisposing factors for the disease (10), while only approximately 6% of colorectal cancers occur in patients with specific hereditary conditions that are known to be predisposing factors for colorectal cancer. Patients without predisposing factors are considered to be at average risk. All other patients are considered to be at moderate or high risk.

Factors that have been associated with an increased risk for the development of colorectal cancer include older age, family history of colorectal cancer, individual history of colorectal cancer or adenomatous polyps, certain hereditary conditions, inflammatory bowel disease, diets that are high in saturated fat and/or low in fiber, excessive alcohol consumption, and sedentary lifestyle (11–22). Obviously, many of these risk factors cannot be changed. Furthermore, the majority of the controllable risk factors (eg, diet, physical inactivity) can require massive efforts to achieve substantial reductions in colorectal cancer risk (23).

Individuals with the highest risk of developing colorectal cancer have either one of two hereditary syndromes or inflammatory bowel disease. Familial adenomatous polyposis syndrome is a genetic condition that affects one in 10,000 people. People with familial adenomatous polyposis invariably develop hundreds of colorectal polyps and will almost certainly develop colorectal cancer unless the entire colon is removed. Hereditary nonpolyposis colorectal cancer syndrome is another genetic condition that, in the absence of multiple polyps, can result in colorectal cancer in affected individuals. Hereditary nonpolyposis colorectal cancer is clinically defined as the presence of colorectal cancer in (a) three or more family members of whom two are first-degree relatives of the third, (b) family members in at least two generations, and (c) one family member who was diagnosed before the age of 50 years (Amsterdam criteria [24]).

Inflammatory bowel disease, including both ulcerative colitis and Crohn disease (which affects the colon and rectum), increases the risk of colorectal cancer. In patients with inflammatory bowel disease, the risk of colorectal cancer depends on the age of onset and the duration and severity of the disease. In general, colorectal cancer develops after at least 8–10 years of colitis (25,26). Although colorectal cancer is more frequently associated with ulcerative colitis than with Crohn disease, the risk associated with both conditions is roughly comparable in terms of age of onset and extent and duration of the inflammatory bowel disease (27). Importantly, cancers that develop in patients with inflammatory bowel disease differ from more typical colorectal cancers in that they generally do not develop from adenomatous polyps, but rather, they develop from areas of high-grade dysplasia. Thus, the greater the extent of mucosal dysplasia, the greater the risk of colon cancer (28–30).

A family history of colorectal cancer in one or more first-degree relatives increases an individual's risk of developing colorectal cancer (10,31–34). In addition, evidence suggests that a family history of breast, ovarian, or endometrial cancer also results in a slightly increased risk of colorectal cancer. Colorectal cancer risk is also increased in people with close relatives in whom adenomatous polyps were diagnosed before the age of 60 years (31). The closer the familial relationship, the greater the number family members affected, and the younger the age of onset, the greater the risk (31). Individuals who have had either colorectal cancer or adenomatous polyps in the past also appear to be at increased risk of developing additional polyps and/or cancers (35–37).

ANATOMIC DISTRIBUTION OF COLORECTAL CANCER

It is interesting to note that the anatomic distribution of colorectal cancer has changed over time (38). In the 1940s, cancer of the rectum and sigmoid colon accounted for 65%–80% of all colorectal cancers, while cancer of the ascending colon and cecum accounted for approximately 10%–15%. However, since 1970, the relative frequency of rectal and sigmoid cancers has decreased to 52%–61%, while the relative frequency of more proximal cancers (ascending colon and cecum) has increased to 19%–24% (39,40). A number of explanations have been proposed to account for these changes. It is likely that improved detection of proximal lesions is responsible to a large extent, in combination with widespread use of sigmoid polypectomy in patients whose distal polyps are detected and removed as a result of routine screening examinations. In addition, more cholecystectomies are performed now than before. Cholecystectomy increases bile salts in the right side of the colon, and the increased use of this procedure has been proposed as a possible explanation for increased development of polyps and cancers in the proximal colon (41).

Both race and sex are known to be independent predictors of cancer location. When black, Asian, and white individuals are compared, Asians tend to have more distal cancers than either blacks or whites, while whites have more distal cancers than blacks (38,42–46). In addition, men have been found to have more distal cancers than women (42,45). The precise explanation for these differences is not known. Nevertheless, the differences may have important consequences on the efficacy of colorectal cancer screening programs, since not all screening tests can be used to detect cancers in all locations equally well.

ADENOMA-CARCINOMA SEQUENCE

It is generally accepted that most cancers of the colon and rectum develop from adenomatous polyps (35,47). Little direct evidence is available, since it would be unethical to leave polyps in situ so that their natural history could be better understood. However, indirect evidence from a variety of sources supports this hypothesis. For example, cancers and polyps have roughly the same anatomic distribution. In addition, cancers rarely develop in the absence of polyps, and the mean age of onset for cancer is greater than the mean age of onset for polyps by several years (48). Furthermore, patients with one or more large (>=1-cm) polyps have been found to be at increased risk of future cancer (49,50), and most of these cancers develop at the site of large polyps that have been left in place (50). Finally, patients with genetic syndromes resulting in increased polyp formation are at greatly increased risk of cancer (34), and the detection and removal of polyps significantly reduces the incidence of colorectal cancer (2,4,51,52).

Fortunately, only a small percentage of all adenomatous polyps progress to cancer. The rate at which this transformation takes place is not precisely known, but it is believed to be somewhat variable. However, it has been estimated that, on average, it takes approximately 10 years for a 1-cm polyp to progress to invasive cancer (2,35,53). Furthermore, it has been estimated that polyps of this size rarely progress to cancer in fewer than 3 years (52,54). The risk that a polyp harbors invasive cancer is related to its size: Polyps smaller than 1 cm are associated with approximately a 1% risk; polyps between 1 and 2 cm, a 10% risk; and polyps larger than 2 cm, a risk of more than 25% (55). The risk of cancer is also related to the villous component of the polyps; in general, villous adenomas have approximately 10 times the risk of cancer compared with that of tubular adenomas of the same size (56).

RATIONALE FOR COLORECTAL CANCER SCREENING

In general, screening for any disease can be justified in the following circumstances: (a) The disease is common and is associated with clinically important morbidity and mortality; (b) screening tests are available, acceptable, feasible, and sufficiently accurate for the detection of early disease; (c) earlier diagnosis and treatment is associated with improved prognosis; and (d) the sum of the benefits associated with screening outweighs the sum of the potential harms and costs. Fortunately, colorectal cancer screening fulfills each of these criteria.

As described previously, colorectal cancer is both common and serious. A variety of screening tests are currently available, are generally acceptable to patients, and are reasonably accurate for the detection of early disease, although accuracy does vary somewhat among the tests. Treatment of patients with advanced colorectal cancer is largely unsuccessful. Furthermore, evidence from a variety of clinical trials suggest that screening and/or removal of adenomatous polyps significantly reduces both the incidence of colorectal cancer and the mortality rate of the disease. Finally, results of several cost-effectiveness analyses have demonstrated that the benefits of screening are achieved at reasonable costs to society.

Unfortunately, most Americans do not currently undergo screening for colorectal cancer. Perhaps the best information on screening rates in the general population is provided by the National Health Interview Survey (57,58). In this survey, personal interviews were conducted in a sample population in the United States. This survey contained questions about cancer screening in 1987 and 1992. Screening rates increased between the two survey dates, but even in 1992, only 17.3% of people aged 50 years or older had undergone fecal occult blood testing in the previous year, and only 9.4% had undergone sigmoidoscopy in the previous 3 years.

It has also been estimated that less than one-third of the patients eligible for colorectal cancer screening have undergone fecal occult blood testing within the past 3 years or colonoscopy (though it is not a recommended screening strategy for average-risk patients) within the last 5 years (59–61). Finally, in a recent study (62), only 40% of average-risk gastroenterologists older than 50 years—a population that would be expected to understand the benefits of screening—underwent colorectal cancer screening with fecal occult blood testing and sigmoidoscopy.

A number of explanations may account for the underutilization of colorectal cancer screening in the population (60). To begin, it is likely that physicians inadequately promote colorectal cancer screening, possibly because of their lack of knowledge or understanding of the risks and benefits of screening. Alternatively, physicians may not recommend screening unless a patient's risk is considered to be sufficient to warrant screening (despite the fact that approximately 75% of cancers occur in patients at average risk for the disease). Some physicians may believe that the benefits of screening are still unproved, or they may be indifferent regarding the need for screening. Finally, given the increasing demands that have been placed on the already busy physician, it is possible that colorectal cancer screening is simply not a priority.

Colorectal cancer screening may also be underutilized because of hesitation or resistance on the part of patients. Patients may not understand the benefits of screening, they may be apathetic, or they may deny that they have any risk for the disease. Patients may also falsely believe that they are no longer at risk of colorectal cancer because of a prior negative result with a screening test. Alternatively, they may be aware of the importance of screening, but they fear either undergoing the tests or the results. Busy schedules and the inconvenience of screening tests may also contribute to underutilization. Last, out-of-pocket expenses may be a factor for some patients, particularly those without health insurance.

OPTIONS FOR COLORECTAL CANCER SCREENING

A number of screening tests are available for the early detection of colorectal cancer. These include digital rectal examination, fecal occult blood testing, flexible and rigid sigmoidoscopy, barium enema examination, colonoscopy, and, most recently, computed tomographic (CT) colonography. CT colonography will be considered in a subsequent article in this series. The remainder are described, including a discussion of their performance characteristics, strengths, and weaknesses.

Digital Rectal Examination
Digital rectal examination can be easily dismissed as an insufficiently sensitive test for the detection of colorectal cancer. The finger used in the examination cannot generally reach even the entire rectum and, obviously, the proximal colon.

Fecal Occult Blood Testing
Fecal occult blood testing is the safest and least expensive of the currently available screening tests. It is a nonspecific test that is used to detect blood in stool. Most colon cancers bleed at least intermittently, so a fecal occult blood test is generally most sensitive for the detection of cancer and much less sensitive for the detection of adenomas, which, in general, do not bleed (63).

Both the sensitivity and specificity of a fecal occult blood test vary with the type of test, that is, rehydrated versus nonrehydrated. Sensitivity is higher and specificity is lower with the rehydrated test. Reported sensitivity for the detection of cancer ranges from approximately 40% to 90%, whereas the sensitivity for the detection of polyps ranges from 10% to 25%. The specificity of fecal occult blood testing ranges from approximately 90% to 98% (depending on the type of test) (4,5,64,65). However, this means that up to 10% of patients who undergo screening will have a false-positive result. Given the extremely low incidence of colorectal cancer in any population that undergoes screening, the overwhelming majority of positive results at fecal occult blood testing will, therefore, be false-positive rather than true-positive. It has been suggested, however, that the high incidence of false-positive test results contributes to the effectiveness of screening fecal occult blood testing, since a positive screening test leads to diagnostic examination (eg, barium enema examination, colonoscopy), which may then lead to the detection of precancerous polyps (66,67).

Four randomized clinical trials have been performed to investigate the benefits of screening with fecal occult blood testing.(4–6,64). These have all been large trials that have included 27,000–150,000 individuals. In these trials, patients were randomly assigned to no screening or screening by means of fecal occult blood testing. In each of these trials, a decrease in the colorectal cancer mortality (of up to 33%) in the population that underwent screening was documented, as well as a stage shift toward more favorable cancers. To our knowledge, these are the only randomized trials to date in which an improvement in the cancer-related mortality from screening with any of the available screening tests has been documented.

Sigmoidoscopy
Next in order of cost and complexity among colorectal cancer screening tests is sigmoidoscopy. Sigmoidoscopy is associated with moderate expense, moderate patient discomfort, and a low risk of complications (approximately one perforation per 10,000 examinations). Sigmoidoscopy can be performed by using either rigid or flexible endoscopes; however, in recent years, flexible sigmoidoscopy has largely replaced rigid sigmoidoscopy. The test is readily available; in many cases, it can be performed in the physician's office. Unlike fecal occult blood testing, sigmoidoscopy permits direct visualization of the distal colon and rectum and has a high sensitivity for the detection of both adenomas and cancers located in the portion of bowel that is visualized. Furthermore, the test permits biopsy and removal of polyps that are detected; therefore, the test can contribute to a reduction in the incidence of colorectal cancer.

An important limitation of sigmoidoscopy is that only the distal colon and rectum are examined; therefore, more proximal lesions may be missed. However, the finding of a distal adenoma may lead to diagnostic colonoscopy and/or barium enema examination either of which may be used to detect additional unsuspected cancers or polyps.

The results obtained with flexible sigmoidoscopy vary with the endoscope used and the skill of the examiner. Two types of flexible sigmoidoscopes are currently in use. The 35-cm scope can access only 50%–75% of the sigmoid colon and can be used to detect only 30%–45% of colorectal polyps and cancers (68). The longer 60-cm scope can be used to examine the entire sigmoid colon in approximately 80% of patients and can, thereby, be used to detect 40%–65% of polyps and cancers (69,70).

Nevertheless, a large number of colonic neoplasms may not be within the reach of either sigmoidoscope. Some of these lesions may be subsequently detected when positive findings at sigmoidoscopy result in a follow-up total colon examination (colonoscopy or barium enema examination). However, approximately 30% of proximal cancers are not associated with a distal adenoma (71–74) and would, thus, be missed at flexible sigmoidoscopy. It should also be noted that some physicians (generally gastroenterologists) routinely perform sigmoidoscopy with the longer colonoscope and then proceed to diagnostic colonoscopy when examination of the sigmoid colon reveals any abnormalities.

Evidence for the benefits of flexible sigmoidoscopy comes from a variety of sources. The proportion of early cancers detected in patients undergoing flexible sigmoidoscopy is increased. These patients have an increased survival compared with that of patients in a nonscreening environment, although most studies have lacked an appropriate comparison group, and, to our knowledge, no randomized study has been performed to compare sigmoidoscopy with no screening. Three case-control studies have been reported (2,3,51). In these, a 60%–80% decrease in the risk of fatal rectosigmoid cancer has been documented. Of these, one (2) included only rigid sigmoidoscopy, while the other (3) included patients undergoing both rigid and flexible sigmoidoscopy. Nevertheless, findings from both studies have been used to support the benefits of screening with flexible sigmoidoscopy.

Barium Enema Examination
Because of the known and increased prevalence of proximal colorectal cancers, increased emphasis has been placed on the need for total colon examination (barium enema examination, colonoscopy) in screening programs. Barium enema examination is a radiologic examination that can be used to detect both adenomas and cancers. It permits examination of the entire colon in approximately 90%–95% of patients (75–77).

Barium enema examination can be performed with either single or double contrast techniques. Because of its relatively high sensitivity, double-contrast barium enema (DCBE) examination is now widely accepted as an effective alternative in colorectal cancer screening. It is associated with moderate patient discomfort, and its cost is between those of sigmoidoscopy and colonoscopy. DCBE examination is associated with a low risk of perforation (approximately one perforation in 25,000 examinations [78]). It results in a low radiation dose of approximately 300–500 mrad (3–5 mGy), which is less than the dose associated with screening mammography at recommended intervals (79).

To our knowledge, no study has been performed to evaluate the accuracy of DCBE examination in a screening population. However, in patients undergoing diagnostic examinations, the reported sensitivity of this test for the detection of cancer ranges from 85% to 90% (80–82). Because of the lack of studies in screening populations, however, the sensitivity for the detection of early cancer is uncertain. Sensitivity for adenomas larger than 1 cm is reported to be 75%–90%, whereas sensitivity for the detection of smaller lesions is reported to be only 50%–80% (83,84). It is important to note, however, that the clinical importance of the detection of adenomas smaller than approximately 0.5–1 cm is unknown, since fewer than 1% of such lesions contain cancer or will ever progress to cancer. Many of the lesions that are missed are detected at subsequent screening examinations before they progress to invasive cancer (50).

Colonoscopy
Colonoscopy is unique among screening tests in that it can be used to examine the entire colon, and, in many cases, it can also be a therapeutic procedure, since many detected polyps or polypoid cancers (depending on their size and stage) may be removed. However, colonoscopy is reported to be incomplete in approximately 5%–15% of patients (71,72,85). Furthermore, colonoscopy is the most invasive and expensive screening test for colorectal cancer. It is associated with moderate patient discomfort. However, this discomfort is often masked by the amnestic effects of the sedative medications that are commonly administered during the procedure. Colonoscopy is associated with the highest risk of perforation of all screening tests (approximately one perforation in 1,000 diagnostic procedures), and approximately one to three per 10,000 patients undergoing colonoscopy will die of complications from the procedure (72,85–87).

As with the barium enema examination, to our knowledge, no study has been performed to assess the performance of colonoscopy in a screening population. Colonoscopy is often assumed to be perfectly sensitive and specific in the portions of the colon traversed by the scope; it has frequently been considered to be the standard in detection studies. However, even large lesions can be missed because of incomplete examinations and/or perceptual errors (88–91). Findings from observational studies suggest that the sensitivity of colonoscopy for cancer detection is approximately 95% (80). However, tandem or sequential-design studies have suggested that the sensitivity of colonoscopy for adenomas larger than 1 cm is only 90%, whereas its sensitivity for the detection of adenomas smaller than 1 cm may be as low as 75% (92,93). Polyps missed at colonoscopy tend to be in predictable locations, such as colonic flexures and/or redundancies (particularly the sigmoid colon or the junction of the sigmoid and descending colon), and splenic and hepatic flexures (88,89).

COST-EFFECTIVENESS ANALYSES

There have been a number of published studies of the cost-effectiveness of screening average-risk individuals for colorectal cancer (94–111). Despite wide variations in strategies modeled and methods and outcome measures used, the consensus from the published studies is that screening for colorectal cancer is cost-effective when it is compared with other screening programs (such as mammography) that are currently used in the United States. However, because different models and modeling assumptions were used and because different strategies were compared, the studies vary widely in their recommended strategies and in their estimates of cost-effectiveness ratios.

In several studies, no screening was compared with annual or biennial fecal occult blood testing, and diagnostic colonoscopy was assumed to be the follow-up examination for a positive fecal occult blood test (99,104,107,108,111). Other studies modeled fecal occult blood testing, either alone or in combination with sigmoidoscopy or barium enema examination, and still others modeled colonoscopy as a stand-alone strategy (102,104,106). For average-risk individuals, estimates of the cost per life-year saved range from $2,057 to $15,168 for fecal occult blood testing every 1 or 2 years (99,107,108,111) versus $9,287 to $22,171 for colonoscopy every 10 years (107). These estimates compare favorably with cited estimates of $8,715 to $50,754 for the cost per life-year saved for screening programs for breast cancer, cervical cancer, or hypertension (112,113). (All costs have been converted to 1998 dollars with the medical care component of the consumer price index and purchasing power parity or exchange rates when necessary.)

Direct comparisons of published studies are difficult, since studies differ in many respects. For example, several studies report conclusions in terms of cost per life saved (102,104), which is difficult to interpret at face value, since saving the life of a 50-year-old typically adds more life-years to a population than does saving the life of a 75-year-old. (Screening is typically suggested for individuals between 50 and 75 years of age.) In addition, the methods used for the estimation of costs and accounting for the relative value of current versus future expenditures for testing and/or treatment differ among the studies.

Furthermore, despite a general consensus that colorectal cancer screening is cost-effective, dissenting opinions are reported in the literature. Criticism is directed at the evidence for the effectiveness of screening, specifically at the uncertainty surrounding the estimates of the characteristics of fecal occult blood testing and the relative reductions in the colorectal cancer mortality ascribed to screening fecal occult blood testing versus follow-up colonoscopy (65). Another criticism is the failure of large trials of fecal occult blood testing to achieve a reduction in overall mortality (despite observed reductions in the colorectal cancer mortality of 15%–33% [114]). However, since the colorectal cancer mortality accounts for only a small percentage (less than 1%) of the overall mortality for this age group (4), this result is not surprising.

EMERGING CONSENSUS

The evolution of colorectal cancer screening has occurred in stages. The first stage was the recognition and acceptance that most colorectal cancers develop from adenomatous polyps. The second stage was the use of small prospective and retrospective studies to evaluate the quality of tests used to diagnose these polyps. The third phase was the demonstration that screening reduces the colorectal cancer mortality rate, with data derived from long-term (4,5,64) or case-control studies (1–3). The final phase is the forging of a national consensus that colon cancer screening should be considered mandatory rather than optional. Several major initiatives have begun to forge a national consensus, and screening by means of DCBE examination is a part of virtually all current initiatives. In this section, we summarize several of the ongoing colorectal cancer screening initiatives.

In March of 1997, the American Cancer Society changed its recommendations on colorectal cancer screening (Table). As stated in the American Cancer Society Cancer Facts and Figures (7), "Beginning at age 50, men and women should have one of the following: a yearly fecal occult blood test plus flexible sigmoidoscopy every 5 years, or colonoscopy every 10 years, or DCBE examination every 5 to 10 years." With this revision of its guidelines, the American Cancer Society introduced the term "total colon examination," or TCE, which emphasizes the importance of an examination of the entire colon (in distinction to indirect or partial examination by using tests such as the fecal occult blood test or sigmoidoscopy) and, thus, emphasizes the value of DCBE examination and colonoscopy.


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  		Summary of American Cancer Society Guidelines for Screening and Surveillance of Colorectal Polyps and Cancer
 
It is important to note, however, that evidence in support of the benefits of screening with fecal occult blood testing alone, sigmoidoscopy alone, or their combination remains stronger than the comparable evidence supporting the use of either barium enema or colonoscopy (9,53). However, because both of these tests are used to examine the entire colon, rather than just the distal rectosigmoid, it is possible to extrapolate from study findings that support screening with sigmoidoscopy to suggest an even greater benefit from screening with barium enema examination or colonoscopy.

The National Colorectal Cancer Roundtable (NCCR) is a national coalition of public, private, and voluntary organizations dedicated to the reduction of the incidence and mortality rate of colorectal cancer in the United States through leadership, strategic planning, advocacy, coordination, and data gathering. The NCCR was first convened in 1997 and was inaugurated and jointly sponsored by the Centers for Disease Control and Prevention and the American Cancer Society. The NCCR has met at yearly intervals since then, with the goal of fostering an increase in colorectal cancer screening rates. At each meeting, a broad cross-section of members of the public has assembled, including physicians representing specialty societies and members of organizations representing the elderly and minorities (including African Americans, Asian Americans, and Native Americans). All federal health agencies and institutes are represented.

The NCCR has established increased participation in screening as its primary mission. Available evidence suggests that screening could have a dramatic effect on colorectal cancer mortality. The NCCR is currently working to understand and remove all barriers to screening. It approaches this analysis from several points of view, including those of society, payers, and providers. For example, one barrier to colonoscopy might be its high initial cost; insurers or physicians paid by means of a capitation system may avoid this test in favor of inexpensive annual fecal occult blood tests even though patients with negative results at colonoscopy need no screening for a decade. This practice occurs because patients frequently switch providers, making it difficult for either the prior insurer (that paid for the test but that may derive no benefits) or for the new insurer (that is likely to benefit because the patient has already undergone screening) to estimate savings from screening tests.

Another barrier to colorectal cancer screening is the nonuniformity of screening recommendations. Virtually every medical society has its own colorectal cancer screening guidelines. Most are similar and usually include recommendations for screening of the average-risk patient with the two tests for which the strongest evidence of effectiveness exists, namely, fecal occult blood testing every year and flexible sigmoidoscopy every 3 or 4 years. However, many of the guidelines go beyond these tests and include options such as colonoscopy and DCBE examination, which are likely to be even more effective. In addition, recommendations for patients at greater than average risk of colorectal cancer vary among medical societies. This multitude of options has created confusion among providers, members of the public, and insurers. Additional barriers are numerous and complex; barriers within radiology almost certainly exist. However, the NCCR, by bringing together representatives of most of the stakeholders in this debate, has the potential to break down many of the existing barriers and to move toward consensus.

The National Council on Quality Assurance has created measurement standards to gauge the effectiveness of health provider organizations. These measurements, called the Health Plan Employers Data and Information Set (HEDIS), are benchmarks against which the effectiveness of providers of health care is measured. These are generally process (rather than outcome) measures, but evidence suggests that the inclusion of mammography screening rates in HEDIS has had a beneficial effect on patient outcomes. Colorectal cancer screening rates are not currently included in the HEDIS measurements. The NCCR and its member organizations have asked the National Council on Quality Assurance to consider the inclusion of colorectal cancer screening in its next revision of HEDIS.

On January 1, 1998, the Health Care Financing Administration of the federal government commenced payment for colorectal cancer screening for all Medicare enrollees older than 50 years (115). For the first time, the federal government thus agreed to cover colorectal cancer screening in all average-risk patients older than 50 years who are covered by Medicare. Previously, Medicare covered testing for only symptomatic or high-risk asymptomatic patients. This change in payment policy was a momentous event for colorectal cancer screening. Although few patients are Medicare enrollees at the age of 50 years, the willingness of the government to extend coverage is evidence of its recognition of the need for colorectal cancer screening. While the Health Care Financing Administration guidelines apply only to payment among Medicare beneficiaries, in reality, they exert an important influence on other payers and on medical practice in general, since they are often adopted by private insurers.

The Health Care Financing Administration rules for average-risk patients offer the choice of three screening strategies. Yearly fecal occult blood testing is covered after the age of 50 years. Flexible sigmoidoscopy or DCBE examination is covered if either is performed at intervals of 48 months or more. Both cannot be covered at the same time. The clinician, therefore, can perform a fecal occult blood test every year and either a DCBE examination or flexible sigmoidoscopic examination every 4 years. No other tests are covered for asymptomatic average-risk individuals.

CHALLENGES AND OPPORTUNITIES IN RADIOLOGY

Colorectal cancer screening presents several opportunities and challenges for radiologists. The national focus on colorectal cancer screening is likely to produce a gradual increase in the demand for barium enema examinations, even if this test merely maintains its current utilization relative to all other screening tests. If barium enema examination proves to be highly effective or cost-effective in ongoing and future studies, the demand for the test will increase even more.

However, before radiologists can expect to participate effectively in any new colorectal cancer screening initiative, they must overcome several major barriers. Radiologists have become increasingly occupied with newer imaging modalities such as CT, magnetic resonance (MR) imaging, and ultrasonography (US). These same modalities, coupled with the increased use of endoscopy, may have resulted in a gradual decline in the skills needed to perform and interpret findings of barium enema examinations. Less attention has been paid in recent years to fluoroscopic procedures and skills, and most younger radiologists are less comfortable performing barium examinations and interpreting the findings. If radiologists are to contribute to the national agenda to decrease colorectal cancer mortality through increased screening efforts, we must strive to maintain and improve our fluoroscopic skills and capacity—at least until an equivalent or better alternative test is available. That alternative test may be a CT (or MR imaging) colonographic examination, a radionuclide test, or even a new and highly specific blood test. In the meantime, however, barium enema examination is a valuable test that can be used to detect and prevent colorectal cancer. We, as radiologists, have an obligation to continue to perform the test at a high and consistent level of quality.

The concept of establishing centers of excellence in colorectal cancer screening has been repeatedly discussed at the NCCR and at a number of regional colorectal cancer workgroups as a method of ensuring all-encompassing quality care for the public. A center of excellence in colorectal cancer screening would be a cohesive unit that offers comprehensive colorectal cancer screening, long-term follow-up, and care. Clinicians at such centers would be skilled in all testing modalities and therapies. Just as breast cancer centers include diagnostic radiologists (with biopsy and localization capacity), surgeons, and medical and radiation oncologists, physicians at the colorectal cancer centers of excellence would need to demonstrate competence in all diagnostic and treatment modalities. However, many details would need to be resolved before such centers could be established and accredited; thus, their potential impact on the field of radiology is unclear.

Clearly, radiologists have something valuable to offer society in the form of barium enema examinations, as shown by every panel that evaluated screening and diagnostic tests. Some barriers that we as a profession must overcome include the widespread belief that our skill in performing the test has eroded. Have we become so preoccupied with our modern tools that we have forgotten to maintain our enthusiasm and skills for performing this robust examination?

CONCLUSION

Screening for colorectal cancer has been identified as a worthwhile investment of societal resources in this country. The government has recognized this. Insurers realize this. The public has and will be told this by public agencies, foundations, and scientists. Radiologists have something important to contribute to this effort today in the form of the barium enema examination. Individual radiologists should prepare to participate in colorectal cancer screening or expect to be left out.

During the next 3 months, a series of articles will be presented to reeducate us and to reignite our enthusiasm. The first article will describe the principles of performing a DCBE examination. The second will describe the diagnostic features of colorectal cancer at DCBE examination. The final article will describe state-of-the-art concepts of CT colonography, which is on its way to becoming a diagnostic and screening tool.

Footnotes

Abbreviations: DCBE = double-contrast barium enema HEDIS = Health Plan Employers Data and Information Set NCCR = National Colorectal Cancer Roundtable

References

  1. Selby JV, Friedman GD, Quesenberry CPJ, et al. Effect of fecal occult blood testing on mortality from colorectal cancer: a case-control study. Ann Intern Med 1993; 118:1-6.[Abstract/Free Full Text]
  2. Selby JV, Friedman GD, Quesenberry CPJ, et al. A case-control study of screening sigmoidoscopy and mortality from colorectal cancer. N Engl J Med 1992; 326:653-657.[Abstract]
  3. Newcomb PA, Norfleet RG, Storer BE, et al. Screening sigmoidoscopy and colorectal cancer mortality. J Natl Cancer Inst 1992; 84:1572-1575.[Abstract/Free Full Text]
  4. Mandel JS, Bond JH, Church TR, et al. Reducing mortality from colorectal cancer by screening for fecal occult blood. N Engl J Med 1993; 328:1365-1371.[Abstract/Free Full Text]
  5. Hardcastle JD, Chamberlain JO, Robinson MH, et al. Randomised controlled trial of faecal-occult-blood screening for colorectal cancer. Lancet 1996; 348:1472-1477.[Medline]
  6. Kronborg O, Fenger C, Olsen J, et al. Randomised study of screening for colorectal cancer with faecal-occult-blood test. Lancet 1996; 348:1467-1471.[Medline]
  7. American Cancer Society. Cancer facts and figures Washington, DC: American Cancer Society, 2000.
  8. Ries LA, Kosary CL, Hankey BF. SEER cancer statistics review Bethesda, Md: National Cancer Institute, 1998; 1973-1995.
  9. Agency for Health Care Policy and Research. Colorectal cancer screening: technical review 1 Rockville, Md: Agency for Health Care Policy and Research, 1998.
  10. Burt RW, Bishop DT, Lynch HT, et al. Risk and surveillance of individuals with heritable factors for colorectal cancer. Bull World Health Organ 1990; 68:655-665.[Medline]
  11. Rose DP, Boyar AP, Wynder EL. International comparisons of mortality rates for cancer of the breast, ovary, prostate, and colon, and per capita food comparison. Cancer 1986; 58:2363-2371.[Medline]
  12. Reddy BS. Dietary fat and its relationship to large bowel cancer. Cancer Res 1981; 41:3700-3705.
  13. Hirayama T, Tannenbaum SR, Reddy BS. A large-scale cohort study on the relationship between diet and selected cancers of the digestive organs. Danbury Rep 1981; 7:409-429.
  14. Willett WC, Stampfer MJ, Colditz GA, et al. Relation of meat, fat, and fiber intake to the risk of colon cancer in a prospective study among women. N Engl J Med 1990; 323:1664-1672.[Abstract]
  15. Neugut AI, Jacobson JS, DeVivo I. Epidemiology of colorectal adenomatous polyps. Cancer Epidemiol Biomarkers Prev 1993; 2:159-176.[Medline]
  16. Cheach PY. Hypothesis for the etiology of colorectal cancer: an overview. Nutr Cancer 1990; 14:5-13.[Medline]
  17. Kampman E, Giovannucci E, van't Veer P, et al. Calcium, vitamin D, dairy foods, and the occurrence of colorectal adenomas among men and women in two prospective studies. Am J Epidemiol 1994; 139:16-29.[Abstract/Free Full Text]
  18. Howe GR, Benito E, Castelleto R, et al. Dietary intake of fiber and decreased risk of cancers of the colon and rectum: evidence from the combined analysis of 13 case-control studies. J Natl Cancer Inst 1992; 84:1887-1896.[Abstract/Free Full Text]
  19. White E, Jacobs EJ, Daling JR. Physical activity in relation to colon cancer in middle-aged men and women. Am J Epidemiol 1996; 144:42-50.[Abstract/Free Full Text]
  20. Slattery ML, Schumacher MC, Smith KR, et al. Physical activity, diet, and risk of colon cancer in Utah. Am J Epidemiol 1988; 128:989-999.[Abstract/Free Full Text]
  21. Whittmore AS, Wu-Williams A, Lee M, et al. Diet, physical activity, and colorectal cancer among Chinese in North America and China. J Natl Cancer Inst 1990; 13:9-17.
  22. Longnecker M, Orza MJ, Adams ME, et al. A meta-analysis of alcoholic beverage consumption in relation to risk of colorectal cancer. Cancer Causes Control 1990; 1:59-68.[Medline]
  23. Doll R, Peto R. The causes of cancer: quantitative estimates of avoidable risks of cancer in the United States today. J Natl Cancer Inst 1981; 66:1191-1308.
  24. Vasen HFA, Mecklin JP, Kahn PM, et al. The international collaborative group on hereditary non-polyposis colon cancer (ICG-NHPCC). Dis Colon Rectum 1991; 34:424-425.[Medline]
  25. Manning AP, Bulgim OR, Dixon MF, et al. Screening by colonoscopy for colonic epithelial dysplasia in inflammatory bowel disease. Gut 1987; 28:1489-1494.[Abstract/Free Full Text]
  26. Brostrom O. Ulcerative colitis in Stockholm County: a study of epidemiology, prognosis, mortality and cancer risk with special reference to a surveillance program. Acta Chir Scand Suppl 1986; 534:1-60.[Medline]
  27. Gillen CD, Walmsley RS, Prior P, et al. Ulcerative colitis and Crohn's disease: a comparison of colorectal cancer risk in extensive colitis. Gut 1994; 35:1590-1592.[Abstract/Free Full Text]
  28. Lennard-Jones JE, Melville DM, Morson BC, et al. Precancer and cancer in extensive ulcerative colitis: findings among 401 patients over 22 years. Gut 1990; 31:800-806.[Abstract/Free Full Text]
  29. Lennard-Jones JE, Connell WR. Surveillance: inflammatory bowel disease. In: Cohen AM, Winawer SJ, eds. Cancer of the colon, rectum, and anus. New York, NY: McGraw-Hill, 1995; 350-370.
  30. Katzka I, Brody RS, Morris E, et al. Assessment of colorectal cancer risk in patients with ulcerative colitis: experience from a private practice. Gastroenterology 1983; 85:22-29.[Medline]
  31. Fuchs CS, Giovannucci EL, Colditz GA, et al. A prospective study of family history and risk of colorectal cancer. New Engl J Med 1994; 331:1669-1674.[Abstract/Free Full Text]
  32. St John JB, McDermott FT, Hopper JL, et al. Cancer risk in relatives of patients with common colorectal cancer. Ann Intern Med 1993; 118:785-790.[Abstract/Free Full Text]
  33. Winawer SJ, Zauber AG, Gerdes H, et al. Risk of colorectal cancer in the families of patients with adenomatous polyps. N Engl J Med 1996; 334:82-87.[Abstract/Free Full Text]
  34. Burt RW, Bishop DT, Cannon L, et al. Dominant inheritance of adenomatous colonic polyps and colorectal cancer. N Engl J Med 1985; 312:1540-1544.[Abstract]
  35. Morson BC. The evolution of colorectal carcinoma. Clin Radiol 1984; 35:425-431.[Medline]
  36. Cali RL, Pitsch RM, Thorson AG, et al. Cumulative incidence of metachronous colorectal cancer. Dis Colon Rectum 1993; 36:388-393.[Medline]
  37. Neugut AI, Lautenbach E, Abi-Rached B, et al. Incidence of adenomas after curative resection for colorectal cancer. Am J Gastroenterol 1996; 91:2096-2098.[Medline]
  38. Demers RY, Severson RK, Schottenfeld D, et al. Incidence of colorectal adenocarcinoma by anatomic subsite. Cancer 1997; 79:441-447.[Medline]
  39. Kelvin FM, Maglinte DDT, Stephens BA. Colorectal carcinoma detected initially with barium enema examination: site distribution and implications. Radiology 1988; 169:1380-1382.
  40. Donald JJ, Burhenne J. Colorectal cancer: can we lower the death rate in the 1990's?. Can Fam Physician 1993; 39:107-114.[Medline]
  41. Giovannucci E, Colditz GA, Stampfer MJ. A meta-analysis of cholecystectomy and risk of colorectal cancer. Gastroenterology 1993; 105:130-141.[Medline]
  42. Hahn DL. Sex and race are risk factors for colorectal cancer within reach of the sigmoidoscopy. J Fam Pract 1990; 30:409-416.[Medline]
  43. Offerhaus GJA, Giardiello FM, Tersmette KF, et al. Ethnic differences in the anatomical location of colorectal adenomatous polyps. Int J Cancer 1991; 49:641-644.[Medline]
  44. Johnson HJ, Margolis I, Wise L. Site-specific distribution of large bowel adenomatous polyps: emphasis on ethnic differences. Dis Colon Rectum 1988; 31:258-260.[Medline]
  45. Nelson RL, Dollear T, Freels S, et al. The relation of age, race, and gender to the subsite location of colorectal carcinoma. Cancer 1997; 80:193-197.[Medline]
  46. Ozick LA, Jacob L, Donelson SS, et al. Distribution of adenomatous polyps in African-Americans. Am J Gastroenterol 1995; 90:758-760.[Medline]
  47. Hill MJ, Morson BC, Bussey HC. Aetiology of adenoma: carcinoma sequence in large bowel. Lancet 1978; 1:245-247.[Medline]
  48. Winawer SJ, Zauber AG, Diaz B. The national polyp study: temporal sequence of evolving colorectal cancer from the normal colon (abstr). Gastrointest Endosc 1987; 33:A167.
  49. Atkin WS, Morson BC, Cuzick J. Long-term risk of colorectal cancer after excision of rectosigmoid adenomas. N Engl J Med 1992; 326:658-662.[Abstract]
  50. Stryker SJ, Wolff BG, Culp CE, et al. Natural history of untreated colonic polyps. Gastroenterology 1987; 93:1009-1013.[Medline]
  51. Muller AD, Sonnenberg A. Prevention of colorectal cancer by flexible endoscopy and polypectomy: a case-control study of 32,702 veterans. Ann Intern Med 1995; 123:904-910.[Abstract/Free Full Text]
  52. Winawer SJ, Zauber AG, Ho MN, et al. Prevention of colorectal cancer by colonoscopic polypectomy. N Engl J Med 1993; 329:1977-1981.[Abstract/Free Full Text]
  53. Winawer SJ, Fletcher RH, Miller L, et al. Colorectal cancer screening: clinical guidelines and rationale. Gastroenterology 1997; 112:594-642.[Medline]
  54. Hoff G, Foertser A, Vatn MN, et al. Epidemiology of polyps in the rectum and colon: recovery and evaluation of unresected polyps 2 years after detection. Scand J Gastroenterol 1986; 21:853-862.[Medline]
  55. Muto T, Bussey HJR, Morson BC. The evolution of cancer of the colon and rectum. Cancer 1975; 36:2251-2270.[Medline]
  56. Stewart ET, Dodds WJ. Polyps. In: Margulis AR, Burhenne HJ, eds. Alimentary tract radiology. St Louis, Mo: Mosby, 1989; 1031.
  57. Anderson LM, May DS. Has the use of cervical, breast, and colorectal cancer screening increased in the United States?. Am J Public Health 1995; 85:840-842.[Abstract/Free Full Text]
  58. Brown ML, Potosky AL, Thompson GB, et al. The knowledge and use of screening tests for colorectal and prostate cancer: data from the 1987 National Health Interview Survey. Prev Med 1990; 19:562-574.[Medline]
  59. Myers RE, Balshem AM, Wolf TA, et al. Adherence to continuous screening for colorectal neoplasia. Med Care 1993; 31:508-519.[Medline]
  60. Vernon SW. Adherence to colorectal cancer screening: a brief overview. Ann NY Acad Sci 1995; 768:292-295.[Medline]
  61. Bat L, Pines A, Ron E, et al. A community-based program of colorectal screening in an asymptomatic population: evaluation of screening tests and compliance. Am J Gastroenterol 1986; 81:647-651.[Medline]
  62. Afridi J, Marshall JB. Do gastroenterologists themselves follow the American Cancer Society recommendations for colorectal cancer screening?. Am J Gastroenterol 1994; 89:2184-2187.[Medline]
  63. Macrae FA, St John JB. Relationship between patterns of bleeding and hemoccult sensitivity in patients with colorectal cancers or adenomas. Gastroenterology 1982; 82:891-898.[Medline]
  64. Kewenter J, Brevinge H, Engarås B, et al. Follow-up after screening for colorectal neoplasms with fecal occult blood testing in a controlled trial. Dis Colon Rectum 1994; 37:115-119.[Medline]
  65. Ahlquist DA. Fecal occult blood testing for colorectal cancer. Gastroenterol Clin N Am 1997; 26:41-55.[Medline]
  66. Lang CA, Ransohoff DF. Fecal occult blood screening for colorectal cancer: is mortality reduced by chance selection for screening colonoscopy?. JAMA 1994; 271:1011-1013.[Abstract]
  67. Ransohoff DF, Lang CA. Small adenomas detected during fecal occult blood test screening for colorectal cancer: the impact of serendipity. JAMA 1990; 164:76-78.
  68. Devesa SS, Chow WH. Variation in colorectal cancer incidence in the Untied States by subsite of origin. Cancer 1993; 71:3819-3826.[Medline]
  69. Selby JV, Friedman GD. US preventative task force. Sigmoidoscopy in the periodic health examination of asymptomatic adults. JAMA 1989; 261:594-601.
  70. Selby JV, Friedman GD, Collen MF. Sigmoidoscopy and mortality from colorectal cancer: the Kaiser Permanente Multiplasic Evaluation study. J Clin Epidemoil 1988; 41:427-434.
  71. Lieberman DA, Smith FW. Screening for colon malignancy with colonoscopy. Am J Gastroenterol 1991; 86:1775-1780.
  72. Rex DK, Lehman GA, Hawes RH, et al. Screening colonoscopy in symptomatic average-risk persons with negative fecal occult blood tests. Gastroenterology 1991; 100:64-67.[Medline]
  73. Kadakia SC, Wrobleski CS, Kadakia AS, et al. Prevalence of proximal colonic polyps in average-risk asymptomatic patients with negative fecal occult blood tests and flexible sigmoidoscopy. Gastrointest Endosc 1996; 44:112-117.[Medline]
  74. Lemmel TG, Haseman JH, Rex DK, et al. Neoplasia distal to the splenic flexure in patients with proximal colon cancer. Gastrointest Endosc 1996; 44:109-111.[Medline]
  75. Bloomfield JA. Reliability of barium enema in detecting colonic neoplasia. Med J Austr 1981; 1:631-633.
  76. Jaramillo E, Slezak P. Comparison between double-contrast barium enema and colonoscopy to investigate lower gastrointestinal bleeding. Gastrointest Radiol 1992; 17:81-83.[Medline]
  77. Brewster NT, Grieve DC, Saunders JH. Double-contrast barium enema and flexible sigmoidoscopy for routine colonic investigation. Br J Surg 1994; 8:445-447.
  78. Blakeborough A, Sheridan MB, Chapman AH. Complications of barium enema examinations: a survey of UK consultant radiologists 1992–1994. Clin Radiol 1992; 52:142-148.
  79. American College of Radiology. CRC screening background report Reston, Va: American College of Radiology, 1998.
  80. 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; 112:17-23.[Medline]
  81. Fork FT, Lindstrom C, Ekelund G. Double contrast examination in carcinoma of the colon and rectum: a prospective clinical series. Acta Radiol 1983; 24:177-188.
  82. Johnson CD, Carlson HC, Taylor WF, et al. Barium enema of carcinoma of the colon: sensitivity of double- and single-contrast studies. AJR Am J Roentgenol 1983; 140:1143-1149.[Abstract/Free Full Text]
  83. Fork FT. Double contrast enema and colonoscopy in polyp detection. Gut 1981; 22:971-977.[Abstract/Free Full Text]
  84. Steine S, Stordahl A, Lunde OC, et al. Double-contrast barium enema versus colonoscopy in the diagnosis of neoplastic disorders: aspects of decision-making in general practice. Fam Pract 1993; 10:288-291.[Abstract/Free Full Text]
  85. Godreau CJ. Office-based colonoscopy in a family practice. Fam Pract Res J 1992; 12:313-320.[Medline]
  86. Jentschura D, Raute M, Winter J, et al. Complications in endoscopy of the lower gastrointestinal tract: therapy and prognosis. Surg Endosc 1994; 8:672-676.[Medline]
  87. Waye JD, Lewis BS, Yessayan S. Colonoscopy: a prospective report of complications. J Clin Gastroenterol 1992; 15:347-351.[Medline]
  88. Laufer I, Smith NCW, Mullens E. The radiological demonstration of colorectal polyps undetected by endoscopy. Gastroenterology 1976; 70:167-170.[Medline]
  89. Miller RE, Lehman G. Polypoid colonic lesions undetected by endoscopy. Radiology 1978; 129:295-297.[Abstract]
  90. Glick SN, Teplick SK, Balfe DM, et al. Large colonic neoplasms missed by endoscopy. AJR Am J Roentgenol 1989; 152:513-517.[Abstract/Free Full Text]
  91. Hixson LJ, Femerty MB, Sampliner RE, et al. Prospective study of the frequency and size distribution of polyps missed by colonoscopy. J Natl Cancer Inst 1990; 82:1769-1772.[Abstract/Free Full Text]
  92. Hixson LJ, Fennerty MB, Sampliner RE, et al. Two year incidence of colon adenomas developing after tandem colonoscopy. Am J Gastroenterol 1994; 89:687-691.[Medline]
  93. Rex DK, Cutler CS, Lemmel GT. Colonoscopic miss rates of adenomas determined by back-to-back colonoscopies. Gastroenterology 1997; 112:24-28.[Medline]
  94. Allison JE, Feldman R. Cost benefits of hemoccult screening for colorectal carcinoma. Dig Dis Sci 1985; 30:860-865.[Medline]
  95. Barry MJ, Mulley AG, Richter JM. Effect of workup strategy on the cost-effectiveness of fecal occult blood screening for colorectal cancer. Gastroenterology 1987; 93:301-310.[Medline]
  96. Brandeau ML, Eddy DM. The workup of asymptomatic patient with a positive fecal occult blood test. Med Decis Making 1987; 7:32-46.
  97. Eddy DM, Nugent FW, Eddy JF, et al. Screening for colorectal cancer in a high-risk population. Gastroenterology 1987; 92:682-692.[Medline]
  98. England WL, Halls JJ, Hunt VB. Strategies for screening for colorectal carcinoma. Med Decis Making 1989; 9:3-13.
  99. Eddy DM. Screening for colorectal cancer. Ann Intern Med 1990; 113:373-384.
  100. Wagner JL, Duffy B, Wadhwa S, et al. Costs and effectiveness of colorectal cancer screening in the elderly. Office of Technology Assessment Washington, DC: United States Congress, 1990.
  101. Wagner JL, Herdman RC, Wadhwa S. Cost-effectiveness of colorectal cancer screening in the elderly. Ann Intern Med 1991; 115:807-817.
  102. Lieberman D. Cost-effectiveness of colon cancer screening. Am J Gastroenterol 1991; 86:1789-1794.[Medline]
  103. Shimbo T, Glick HA, Eisenberg JM. Cost-effectiveness analysis of strategies for colorectal cancer screening in Japan. Int J Technol Assess Health Care 1994; 10:359-375.[Medline]
  104. Lieberman DA. Cost-effectiveness model for colon cancer screening. Gastroenterology 1995; 109:1781-1790.[Medline]
  105. Salkeld G, Young G, Irwig L, et al. Cost-effectiveness analysis of screening for faecal occult blood testing for colorectal cancer in Australia. Aust NZ J Public Health 1996; 20:138-143.[Medline]
  106. Geul KW, Bosman FT, Van Blakenstein M, et al. Prevention of colorectal cancer. Scand J Gastroenterol 1997; 223(suppl 32):79-87.
  107. Glick S, Wagner JL, Johnson CD. Cost-effectiveness of double-contrast barium enema in screening for colorectal cancer. AJR Am J Roentgenol 1998; 170:629-636.[Free Full Text]
  108. Gyrd-Hansen D. Fecal occult blood tests: a cost-effectiveness analysis. Int J Technol Assess Health Care 1998; 14:290-301.[Medline]
  109. Gyrd-Hansen D, Sogaard J, Kronborg O. Colorectal cancer screening: efficiency and effectiveness. Health Econ 1998; 7:9-20.[Medline]
  110. Norum J. Prevention of colorectal cancer: a cost-effectiveness approach to a screening model employing sigmoidoscopy. Ann Oncol 1998; 9:613-618.[Abstract/Free Full Text]
  111. Whynes DK, Nielson AR, Walker AR, et al. Fecal occult blood screening for colorectal cancer: is it cost-effective?. Health Econ 1998; 7:21-29.[Medline]
  112. Garber AM, Phelps CE. Economic foundation of cost-effectiveness analysis. J Health Econ 1997; 16:1-31.[Medline]
  113. Brown ML, Fintor L. Cost-effectiveness of breast cancer screening: preliminary results of a systematic review of the literature. Breast Cancer Res Treat 1993; 25:113-118.[Medline]
  114. Kronborg O, Fenger C. Prognostic evaluation of planned follow-up in patients with colorectal adenomas: an interim report. Int J Colorectal Dis 1987; 2:203-207.[Medline]
  115. 62 Federal Register 211 1997.



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