Background and Methods The clinical significance of a distalcolorectal polyp is uncertain. We determined the risk of advancedproximal neoplasia, defined as a polyp with villous features,a polyp with high-grade dysplasia, or cancer, among personswith distal hyperplastic or neoplastic polyps as compared withthe risk among persons with no distal polyps. We analyzed datafrom 1994 consecutive asymptomatic adults (age, 50 years orolder) who underwent colonoscopic screening for the first timebetween September 1995 and December 1998 as part of a programsponsored by an employer. The location and histologic featuresof all polyps were recorded. Colonoscopy to the level of thececum was completed in 97.0 percent of the patients.
Results Sixty-one patients (3.1 percent) had advanced lesionsin the distal colon, including 5 with cancer, and 50 (2.5 percent)had advanced proximal lesions, including 7 with cancer. Twenty-threepatients with advanced proximal neoplasms (46 percent) had nodistal polyps. The prevalence of advanced proximal neoplasiaamong patients with no distal polyps was 1.5 percent (23 casesamong 1564 persons; 95 percent confidence interval, 0.9 to 2.1percent). Among patients with distal hyperplastic polyps, thosewith distal tubular adenomas, and those with advanced distalpolyps, the prevalence of advanced proximal neoplasia was 4.0percent (8 cases among 201 patients), 7.1 percent (12 casesamong 168 patients), and 11.5 percent (7 cases among 61 patients),respectively. The relative risk of advanced proximal neoplasia,adjusted for age and sex, was 2.6 for patients with distal hyperplasticpolyps, 4.0 for those with distal tubular adenomas, and 6.7for those with advanced distal polyps, as compared with patientswho had no distal polyps. Older age and male sex were associatedwith an increased risk of advanced proximal neoplasia (relativerisk, 1.3 for every five years of age and 3.3 for male sex).
Conclusions Asymptomatic persons 50 years of age or older whohave polyps in the distal colon are more likely to have advancedproximal neoplasia than are persons without distal polyps. However,if colonoscopic screening is performed only in persons withdistal polyps, about half the cases of advanced proximal neoplasiawill not be detected.
The clinical significance of distal colorectal polyps dependson two factors: whether the polyps are associated with advancedproximal neoplasms, and whether polyps with histologic featuresof advanced neoplasia (e.g., villous features) are clinicallyimportant. Although Stryker et al. reported that large polyps(>10 mm in diameter) left intact progress to colorectal cancerat a rate of about 1 percent per year,1 it is unclear whethersmaller polyps with histologic features of advanced neoplasiahave a similar natural history. If early detection of such lesionsis desirable, then the ability to estimate the risk of advancedproximal neoplasia with precision may be important both fordeciding which patients should undergo examination of the proximalcolon after sigmoidoscopic screening and for evaluating otherscreening strategies.
Previous studies of the association between polyps in the distalcolon and advanced proximal neoplasia have lacked control groupsof persons with no distal abnormalities,2,3,4,5 making it difficultto identify risk factors for advanced proximal neoplasia. Furthermore,these studies have varied with respect to features that canaffect the outcome, including the sample size and the criteriafor classifying distal lesions (i.e., according to their size,number, location, or histologic features). Differences in reportedrisks have led to conflicting recommendations for the use ofcolonoscopy according to distal findings, particularly for patientswith distal tubular adenomas, with important implications forthe case of individual patients as well as for guidelines forcolorectal-cancer screening.2,3,4,5
We analyzed data from a large cohort of persons at average riskwho underwent colonoscopic screening for colorectal cancer.Our primary objective was to determine the relative risk ofadvanced proximal neoplasia in patients with distal polyps,either hyperplastic or neoplastic, as compared with personswith no distal polyps. A secondary objective was to determinethe risk of large proximal neoplasms (10 mm in diameter) accordingto the distal findings.
Methods
Study Design
We performed a cross-sectional analysis of consecutive asymptomaticadults, 50 years of age or older, who underwent colonoscopicscreening for the first time between September 1995 and December1998. The study was approved by the institutional review boardof Indiana University at Indianapolis.
Screening Program
In September 1995, Eli Lilly, which has its own health insuranceplan for employees, retirees, and their dependents, began providingcolonoscopic screening as a benefit. Persons 40 years of ageor older receive a brochure about the screening program andare encouraged to call a toll-free number for more informationor to make an appointment to be screened. A telephone interviewis used to establish that persons who call to make an appointmentfor screening are asymptomatic (e.g., they report no visiblerectal bleeding, no recent change in bowel habits, and no recentor current lower abdominal pain) and have no personal historyof colorectal cancer, colorectal polyps, or inflammatory boweldisease. Thirty-six board-certified gastroenterologists andcolorectal surgeons practicing in central Indiana participatein the screening program.
Study Procedures and Definitions
Polyethylene glycol lavage solution was used for bowel preparation.Fecal occult-blood testing was not performed before colonoscopicscreening, and information on the presence or absence of a familyhistory of colorectal cancer and the results of prior screeningor diagnostic colorectal evaluations was not available, sincesuch information is not routinely recorded.
During colonoscopy, the location and size of all polyps weredetermined before they were removed. Pathological specimenswere evaluated by one of three board-certified pathologists,who classified polyps according to the criteria establishedby the World Health Organization.6
For the purpose of our analysis, the boundary between the proximalcolon and the distal colon was defined as the junction of thesplenic flexure and the descending colon, as assessed by theendoscopist. In the case of patients with more than one polypin either the proximal or distal segment of the colon, the mostadvanced lesion in that segment was included in the analysis.The size of the polyp was estimated either with the use of open-biopsyforceps or on the basis of clinical judgment.
Distal and proximal findings were categorized as indicatingnormal mucosa (no polyps), hyperplastic polyps, tubular adenomas,or advanced neoplasms. An advanced neoplasm was defined as apolyp or polypoid lesion with villous features, a polyp or polypoidlesion with high-grade dysplasia, or cancer. Findings such aslipomas, lymphoid aggregates, chronic nonspecific inflammation,and inflammatory or juvenile polyps were categorized as indicatingnormal mucosa. No specimens were considered to be nondiagnostic.
Statistical Analysis
The prevalence of both advanced proximal neoplasms and largeproximal neoplasms was calculated on the basis of the distalcolorectal findings. The unadjusted relative risk of each distaland proximal finding was calculated for men as compared withwomen.7 Multivariate logistic-regression analysis was used toestimate the adjusted relative risk of advanced proximal neoplasiaand large proximal neoplasms (10 mm in diameter), with the useof age, sex, and distal colorectal findings as independent variables.8For each distal finding, the "number needed to screen" was determined.Conceptually similar to the "number needed to treat,"9 the numberneeded to screen is the number of persons with a particulardistal finding who would have to undergo colonoscopy in orderto detect one advanced proximal neoplasm. Analyses were performedwith SPSS for Windows software (version 9.0, SPSS, Chicago).
Results
From September 1995 through December 1998, a total of 2686 personsunderwent colonoscopic screening. We excluded from the analysis692 persons who were less than 50 years old. The study cohortthus consisted of 1994 persons. Their mean (±SD) agewas 59.8±8.3 years, and 58.9 percent were men (mean age,59.6±8.3 years). The mean age of the women was 60.1±8.4years. Colonoscopy to the cecum was performed in 97.0 percentof patients.
A total of 12 cancers were detected: 8 in men and 4 in women;their mean age was 69.8±10.0 years. Seven patients hadcancers in the proximal portion of the colon; in three of theseven, there were associated distal lesions (adenomas in twopatients and a hyperplastic polyp in one). Five of the 12 patientshad carcinoma in situ, 1 had a Dukes' stage A lesion, 4 hadDukes' stage B lesions, and 2 had Dukes' stage C lesions.10There were no deaths related to colonoscopy. One patient hada colonic perforation that was managed medically. Three patientswho had bleeding after polypectomy went to an urgent care centeror emergency room for evaluation; none required transfusionor surgery.
Distal and proximal findings are shown in Table 1. No polypswere present in the distal colon in 78.4 percent of the patients(mean age, 60.0±8.3 years). Hyperplastic polyps, tubularadenomas, and advanced neoplasms were present in the distalcolon in 10.1 percent, 8.4 percent, and 3.1 percent of the patients,respectively. Men were more likely than women to have hyperplasticpolyps (unadjusted relative risk, 1.49; 95 percent confidenceinterval, 1.12 to 1.97), tubular adenomas (unadjusted relativerisk, 1.54; 95 percent confidence interval, 1.13 to 2.11), andadvanced neoplasms (unadjusted relative risk, 2.39; 95 percentconfidence interval, 1.32 to 4.31).
Table 1. Findings in the Distal and Proximal Colon in the Cohort of 1994 Patients.
No polyps were present in the proximal colon in 84.6 percentof the cohort (mean age, 59.8±8.2 years) (Table 1). Hyperplasticpolyps were present in 3.6 percent, tubular adenomas in 9.3percent, and advanced neoplasms in 2.5 percent. Men were morelikely than women to have tubular adenomas (unadjusted relativerisk, 2.3; 95 percent confidence interval, 1.7 to 3.2) and advancedneoplasms (unadjusted relative risk, 3.7; 95 percent confidenceinterval, 1.8 to 8.0).
The prevalence of advanced proximal neoplasia according to thefindings in the distal colon is shown in Table 2. Among the1564 persons with no distal polyps, the prevalence of proximalneoplasia was 1.5 percent (95 percent confidence interval, 0.9to 2.1 percent), and the prevalence increased linearly amongpersons with distal hyperplastic polyps (4.0 percent), tubularadenomas (7.1 percent), and advanced neoplasms (11.5 percent).The proportions were essentially the same when advanced proximalneoplasms and large proximal neoplasms were considered together.Twenty-three of the 50 patients with advanced proximal neoplasia(46.0 percent) had no polyps in the distal colon. Had these23 patients undergone screening sigmoidoscopy, their proximalneoplasms would not have been detected, because of the absenceof distal polyps.
Table 2. Prevalence of Advanced Proximal Neoplasms According to the Distal Findings.
Table 2 also shows the relative risk of advanced proximal neoplasia,adjusted for age and sex, according to the distal findings,with patients who had no distal polyps serving as the referencegroup. The magnitude of the risk was related to the histologicfeatures of the distal lesion.
The size of a distal adenoma alone was unrelated to the riskof advanced proximal neoplasia. Thirteen of 124 patients withdistal adenomas that were 1 to 5 mm in diameter had advancedproximal neoplasia (10.5 percent; 95 percent confidence interval,5.7 to 17.3 percent). Advanced proximal lesions were detectedin 2 of 72 patients with adenomas that were 6 to 9 mm in diameter(2.8 percent; 95 percent confidence interval, 0.3 to 6.6 percent)and in 4 of 26 with distal adenomas that were 10 mm or morein diameter (15.4 percent; 95 percent confidence interval, 4.4to 34.9 percent), respectively.
The prevalence of large proximal neoplasms according to thedistal findings is shown in Table 3. Despite the small numberof patients with large lesions, the risk of a large proximalneoplasm was significantly associated with the histologic stageof the distal lesion (two-tailed P value for trend, 0.02). Theconfidence intervals for the proportions indicate that the riskof large proximal neoplasms was greater for patients with distaltubular adenomas or advanced neoplasms than for those with distalhyperplastic polyps or no distal polyps. Table 3 also showsthe adjusted relative risk of a large proximal neoplasm accordingto the distal findings, with persons who had no distal polypsserving as the reference group. The presence of distal neoplasiaincreased the age- and sex-adjusted relative risk of a largeproximal neoplasm.
Table 3. Prevalence of Large Proximal Neoplasms According to the Distal Findings.
Multivariate analysis showed that after adjustment for sex anddistal findings, age was significantly associated with the riskof advanced proximal neoplasia, with a relative risk of 1.3(95 percent confidence interval, 1.3 to 1.4) for every successivefive-year interval between the ages of 50 and 80 years. Likewise,male sex, adjusted for age and distal findings, increased therisk of advanced proximal neoplasia by 3.3 (95 percent confidenceinterval, 1.5 to 7.1).
Discussion
If there were a reliable distal marker for clinically importantproximal neoplasia (i.e., a sentinel lesion) or if normal findingsin the distal colon were a reliable marker for the absence ofclinically important proximal neoplasia, then sigmoidoscopicexamination of the distal colon and rectum would help determinewhich persons should undergo examination of the proximal colon.
In our study, a polyp of any size or type in the distal colonwas associated with an increased risk of histologically advancedproximal neoplasia. The magnitude of the risk was proportionalto the histologic features of the distal lesion. The risk ofa large proximal neoplasm was similarly related to the histologicfeatures of polyps in the distal colon.
Because previous research has suggested that the histologicfeatures of distal polyps may be a better marker for advancedproximal neoplasia than their size11 and because the measurementof a polyp through the endoscope may be inaccurate,12 we definedan advanced neoplasm on the basis of histologic findings insteadof size. To make our findings comparable with those of otherstudies, however,2,3,4,5 we also considered the relation betweendistal polyps and the combination of histologically advancedneoplasms and large tubular adenomas (10 mm in diameter) inthe proximal colon. Because this relation was no different fromthat between distal polyps and histologically advanced proximalneoplasms alone, we have presented the results only for thedefinition of advanced neoplasm that we consider to be the morereliable of the two definitions.
In addition to distal polyps, we found that age was an importantpredictor of risk. For every five-year interval between theages of 50 and 80 years, the risk of advanced proximal neoplasiaincreased by 32 percent. Few data are available to assess ageas an independent risk factor for advanced proximal neoplasia.Levin and colleagues found that an age of more than 65 yearswas an independent risk factor for advanced proximal neoplasia.5In a study of colonoscopic screening among 621 asymptomaticpersons who were 50 to 75 years old and who had negative fecaloccult-blood tests, Rex and colleagues found that each five-yearincrease in age increased the odds of colonic neoplasia of anykind by 1.36.13
In our study, men were more likely than women to have both proximaland distal neoplasms and were more than three times as likelyto have advanced proximal neoplasms, after adjustment for ageand distal findings. Although men are known to be at increasedrisk for colorectal neoplasia, the effect of sex apart fromage and distal findings has been uncertain.11,14
The prevalence of advanced proximal neoplasia in our patientswith distal hyperplastic polyps was 4.0 percent (95 percentconfidence interval, 1.3 to 6.7 percent). Although the 95 percentconfidence interval for this estimate overlaps that for personswith no distal polyps, the relative risk of advanced proximalneoplasia, adjusted for age and sex, in patients with distalhyperplastic polyps as compared with the patients who had nodistal polyps was 2.6 (95 percent confidence interval, 1.1 to5.9). In part because of small samples, studies of the riskof proximal neoplasia in asymptomatic persons with distal hyperplasticpolyps have had inconsistent findings. The risk of a proximalneoplasm of any size has ranged from 15 to 32 percent.15,16,17,18More important, the risk of advanced proximal neoplasia andthe risk of large proximal neoplastic polyps have not been assessed.Otori and colleagues found K-ras mutations in 47 percent ofhyperplastic polyps, suggesting that they could be precursorsof neoplasia.19 In the light of practice guidelines suggestingthat hyperplastic polyps are not im-portant20,21 and the needto consider previous findings in the process of interpretingnew data,22 the importance of hyperplastic polyps remains uncertainand must be clarified by further research.
The efficiency of sigmoidoscopic screening in detecting proximallesions can be assessed by calculating the number needed toscreen — that is, the number of persons who would haveto undergo sigmoidoscopic screening in order to detect one advancedproximal neoplasm. As the criterion for performing colonoscopyis relaxed (i.e., from the most stringent criterion of an advanceddistal neoplasm to the criteria of a distal tubular adenomaor advanced neoplasm, any distal polyp, and finally, no polyp),the number needed to screen increases substantially (Table 4).However, the proportion of patients with advanced proximal neoplasiaalso increases. Furthermore, even when colonoscopy is performedfor any distal polyp, nearly half the cases of advanced proximalneoplasia are missed. These data indicate that a substantialproportion of advanced proximal neoplasms are not associatedwith any distal sentinel lesion. Physicians and policy makerscould use this information to determine the appropriate thresholdfor performing a full colonoscopic examination. Although ourdata may be useful for deciding which screening techniques arebest, other information is also important, such as the expenseand complications of colonoscopy, the need for and frequencyof repeated examinations, coexisting disease in patients undergoingscreening, and the natural history of histologically advancedneoplasms.
Table 4. Number Needed to Screen According to the Distal Finding Used as a Criterion for Colonoscopy.
The limitations of our study require comment. Despite the colonoscopicscreening of 1994 persons, only 50 advanced proximal neoplasmswere found. The small number of advanced and large proximalneoplasms precluded certain subgroup analyses. This limitationis not unique to our study. Some investigators have suggestedthat the size and number of distal tubular adenomas may affectthe risk of proximal neoplasia.2,3,4 In our study, only 12 ofthe 168 persons with distal tubular adenomas had advanced proximalneoplasms. The small size of this subgroup precluded the detectionof any but the largest differences. Furthermore, we did notfind a significant association between the risk of advancedproximal neoplasia and the size of a distal adenoma, in contrastto the results reported by Read and colleagues.2 Yet becausethe two studies had small numbers of patients, with overlappingconfidence intervals for each category of lesions, the resultsof the two analyses are not statistically different. Wide confidenceintervals as a result of the small numbers of advanced proximallesions account at least in part for the paradox of qualitativelydifferent yet statistically similar findings among studies.
Both in our study and in previous studies, limited clinicalinformation was available to supplement the endoscopic informationprovided by the screening examinations. Individual risk estimatesfor advanced proximal neoplasia might be derived from such informationas race, body-mass index, the presence or absence of a familyhistory of colorectal neoplasia, and the results of any previouscolorectal screening and diagnostic tests. Although severalgroups have investigated the risk of proximal neoplasia on thebasis of distal findings alone,2,3,4,5,23,24,25,26 future studiesshould evaluate the risk by incorporating additional clinicalinformation.
In summary, we found that increasing age, male sex, and thepresence of polyps in the distal colon were independent riskfactors for advanced proximal neoplasms in persons who were50 years of age or older. Although our results are consistentwith those of other studies with respect to the importance ofadvanced distal neoplasms as a marker of proximal neoplasia,our findings raise questions about the possible additional importanceof hyperplastic polyps. Like other investigators,27,28 we foundthat almost half the patients with advanced proximal neoplasmshad no distal lesions. The current strategy of deciding whoshould undergo colonoscopy solely according to the findingsin the distal colon should be reconsidered.
Supported in part by grants from the Walther Cancer Institute,Indianapolis, and the National Institute of Diabetes and Digestiveand Kidney Diseases (K24 DK02756-02).
We are indebted to the following members of the Lilly ColorectalCancer Prevention Program: Kathy Anderson, R.N., David Bash,M.D., Diane Batza, R.N., Jeffery Bilotta, M.D., Robert Bishop,M.D., Gary Bolinger, M.D., Lawrence Born, M.D., E. David Brown,M.D., Galantin Bryan, J. Scott Buckley, M.D., Janet Burson,R.N., Robert Callon, M.D., Gene Chiao, M.D., Charles Cline,M.D., Sue Cornelius, R.N., Michael Elmore, M.D., William Erdel,M.D., Paul Frederick, M.D., John Geneczko, M.D., Elizabeth Glowinski,R.N., Debra Helper, M.D., David Hollander, M.D., James Jacob,M.D., Olaf Johansen, M.D., Joseph Katz, M.D., Paul Kwo, M.D.,Frederick Lane, M.D., Gregory Lemmel, M.D., Margaret Lockard,R.N., Mark Lybik, M.D., Stephen Mahoney, M.D., Michael Manbeck,M.D., James McGill, M.D., Donald McGovern, Jr., M.D., BeckyMellon, R.N., Janet Miller, R.N., Katherine O'Conner, M.D.,Thomas O'Conner, M.D., Patrick Park, M.D., Scott Pittman, M.D.,David Pound, M.D., Phyllis Quintana, Douglas Rex, M.D., DonaldShook, M.D., William Sobat, M.D., Daniel Stanley, M.D., FrankTroiano, M.D., Benjamin Upchurch, M.D., Max Warner, M.D., andMaurits Wiersema, M.D.
Source Information
From the Departments of Medicine, Indiana University Medical Center and Roudebush Veterans Affairs Medical Center (T.F.I., C.Y.L.); the Indianapolis Gastroenterology Research Foundation (D.R.W., J.D.R.); and Eli Lilly (G.N.L.) — all in Indianapolis; and the Department of Medicine, University of North Carolina at Chapel Hill, Chapel Hill (D.F.R.).
Address reprint requests to Dr. Imperiale at Indiana University Medical Center, Division of Gastroenterology, 975 W. Walnut St., IB-424, Indianapolis, IN 46202-5121.
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10 mm in diameter) according to the distal findings. 
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