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Review Article |

Risk of Proximal Colon Neoplasia With Distal Hyperplastic Polyps:  A Meta-analysis FREE

Otto S. Lin, MD, MSc; Lauren B. Gerson, MD, MSc; Maw-Soan Soon, MD; Drew B. Schembre, MD; Richard A. Kozarek, MD
[+] Author Affiliations

Author Affiliations: Gastroenterology Section, Virginia Mason Medical Center, Seattle, Wash (Drs Lin, Schembre, and Kozarek); Gastroenterology Division, Stanford University Medical Center, Stanford, Calif (Dr Gerson); and Gastroenterology Division, ChangHua Christian Medical Center, ChangHua City, Taiwan (Drs Lin and Soon).


Arch Intern Med. 2005;165(4):382-390. doi:10.1001/archinte.165.4.382.
Text Size: A A A
Published online

Background  Most guidelines for colorectal cancer screening do not consider distal hyperplastic polyps (HPs) to be markers for proximal colon neoplasia. However, many studies have shown an increased risk of proximal neoplasia (PN) in patients with distal HPs. We performed a systematic review to assess the association between distal HPs and PN.

Methods  We identified studies that compared the prevalence of PN and proximal advanced neoplasia in patients with distal HPs vs controls. Two masked investigators extracted data on individuals with distal HPs, distal adenomas, or no distal polyps. Using the DerSimonian and Laird method, we calculated summary risk ratios. Extensive subgroup analysis was performed.

Results  The prevalence of PN and proximal advanced neoplasia in persons with distal HPs was 26.0% and 4.4%, respectively. In studies comparing the risk of PN in patients with distal HPs vs those with no distal polyps, the summary risk ratio was 1.81 (95% confidence interval, 1.20-2.73). However, this increased risk disappeared if only high-quality studies on screening patients were considered. The risk ratio was 0.69 (95% confidence interval, 0.60-0.80) when comparing the risk of PN in those with distal HPs vs those with distal adenomas.

Conclusions  Overall, patients with distal HPs have an intermediate risk of PN compared with those with distal adenomas or no distal polyps; however, in asymptomatic screening individuals, there is no increased risk of PN or proximal advanced neoplasia. The discovery of HPs on screening flexible sigmoidoscopy should not automatically prompt follow-up colonoscopy.

Figures in this Article

Guidelines from medical societies recommend screening for colorectal cancer (CRC) in average-risk individuals by using flexible sigmoidoscopy (FS) or other methods.14 Most of these guidelines do not consider a distal hyperplastic polyp (HP) to be a marker for proximal colon neoplasia24; in other words, the discovery of a distal HP on screening FS would not be an indication for colonoscopy. However, HPs may have neoplastic potential because they may contain genetic changes seen in CRC, such as K-ras mutations and microsatellite instability,57 and are associated with epidemiologic risk factors linked to CRC, including tobacco use, high dietary fat intake, and lack of dietary fiber.8,9 During the past 15 years, studies comparing the prevalence of proximal neoplasia (PN) in patients with distal HPs, distal tubular adenomas (TAs), and no distal polyps have reported conflicting results. The purpose of this systematic review is to analyze the available data on the risk of PN in individuals with distal HPs, a clinically important issue regarding whether patients with HPs found on FS should be referred for colonoscopy.

STUDY IDENTIFICATION

We searched the MEDLINE (PubMed) and EMBASE databases (December 1966 to March 2004) using a combination of the title and abstract terms hyperplastic and hyperplasia with any of the following title and abstract terms: polyp, adenoma,adenomatous, neoplasm, neoplasia, neoplastic, sigmoidoscopy, proctoscopy, endoscopy, colonoscopy, cancer, and screening. Using the same terms, we searched the indexes of abstracts from meetings of the American Gastroenterological Association, the American College of Gastroenterology, and the American Society of Gastrointestinal Endoscopy (January 1992 to December 2003). Abstracts for these conferences are published in the journals Gastroenterology, American Journal of Gastroenterology, and Gastrointestinal Endoscopy, respectively. In addition, we manually reviewed citations in all included articles, editorials, and review articles on CRC screening published between January 1992 and December 2003 in major gastroenterology, internal medicine, and oncology journals (American Journal of Gastroenterology, Annals of Internal Medicine, British Medical Journal, Cancer, Gastroenterology, Gastrointestinal Endoscopy, Gut, Journal of the American Medical Association, The Lancet, andthe New England Journal of Medicine). Last, we also manually reviewed citations in the pertinent chapters of important gastroenterology textbooks.1012

This search strategy was designed to be highly sensitive (but with low specificity). We manually reviewed the titles of all retrieved studies, and clearly irrelevant ones were excluded. We then reviewed the abstracts of the remaining, potentially relevant studies. After excluding inappropriate studies based on predefined exclusion criteria (see the following subsection), the full texts of the remaining studies were reviewed to confirm eligibility. Studies that were ultimately excluded after a full text review are individually described (see the “Results” section), along with reasons for exclusion.

INCLUSION AND EXCLUSION CRITERIA

We required eligible studies to be prospective, retrospective, or cross-sectional analyses designed to examine the prevalence of PN in patients with distal HPs compared with that in patients with distal TAs and patients with no distal polyps. Eligible studies were required to have been published as full articles in a peer-reviewed journal, as abstracts from a national or international conference, or as part of a major gastroenterology textbook. Studies published in non-English languages were eligible. Studies that included patients with the following exclusion criteria were excluded: a history of CRC, inflammatory bowel disease, or a family history of polyposis or hereditary nonpolyposis CRC syndromes. Case reports or series and autopsy studies were excluded. Studies involving symptomatic patients were eligible but were subjected to subgroup analysis.

DATA ABSTRACTION AND ANALYSIS

Two masked investigators (O.S.L. and L.B.G.) independently abstracted data on the prevalence of PN and proximal advanced neoplasia (PAN) of the colon in 3 groups of patients: those with distal colonic HPs but no distal TAs, those with distal TAs with or without distal HPs, and those with no distal polyps. An advanced lesion was defined as any neoplastic polyp measuring 1 cm or greater or with villous, dysplastic, or malignant features. Proximal neoplasia included small proximal adenomas and PAN. The distal TA group excluded patients with distal advanced neoplasia or cancers (because such patients will always be referred for colonoscopy). The no distal polyp group included individuals with nonneoplastic, nonhyperplastic lesions, such as inflammatory polyps, lymphoid hyperplasia, and polyps with “normal histologic features.” The same customized data abstraction form was used by both investigators. Disagreements were resolved by a second review and consensus. We attempted to contact study authors by telephone, mail, or e-mail to clarify ambiguous data or to fill in missing data.

Two outcomes were considered: PN (including advanced lesions) and PAN. For each outcome, we calculated the summary prevalence and the summary risk ratio (RR), with 95% confidence intervals (CIs), using the DerSimonian and Laird method based on a random-effects model. We tested for heterogeneity by calculating a Q statistic in the standard manner. Data analysis was performed using statistical analysis software (Comprehensive Meta-Analysis 1.023; Biostat Inc, Englewood, NJ, and SPSS version 11.0; SPSS Inc, Chicago, Ill).

SUBGROUP AND SENSITIVITY ANALYSIS

To assess the impact of the meta-analysis methods, we also calculated summary RRs using fixed-effects model techniques, that is, the inverse variance and Mantel-Haenszel methods. Because the data were expected to be heterogeneous, extensive subgroup analysis was performed using the following moderator variables: (1) patient symptoms (some studies included only asymptomatic screening individuals, whereas others included symptomatic patients [eg, diarrhea and hematochezia] undergoing diagnostic colonoscopy); (2) study design (in some studies, colonoscopy was performed on all patients regardless of distal findings [“universal colonoscopy” design], whereas in others, patients first underwent FS, with colonoscopy performed only in those found to have distal polyps of any type [“nonuniversal colonoscopy” design]; in the latter group, biopsy of the distal polyp was often not performed until the time of colonoscopy); (3) publication date (studies were stratified according to whether they were published after 1992 [this date was chosen because a preliminary review showed that approximately half the studies were published after 1992]); (4) sample size (studies were stratified according to whether they enrolled >300 total patients); (5) demarcation definition (some studies defined the demarcation between the proximal and distal colon as the splenic flexure or the descending sigmoid junction, whereas others defined it as the extent of FS); (6) distal polyp size (some studies restricted themselves to subjects with distal polyps <5 mm, whereas others had no size restrictions); (7) age (some studies restricted participants to those ≥50 years); (8) family history (some studies included individuals with a family history of CRC, some excluded such patients, and others did not comment on family history); and (9) study quality. Unlike randomized controlled trials, observational studies do not have commonly used and well-validated quality scoring systems.13 Therefore, we created a simple scoring system for this meta-analysis. We assigned each study a score based on the type of publication (full article vs abstract), patient symptoms, study design, comparison groups, and sample size. Studies that were published in full, that included only asymptomatic screening patients, that featured a universal colonoscopy design, that included all 3 comparison groups, and that had 300 or more participants received 1 point for each category (for a maximum score of 5). Studies that were published as abstracts, that included symptomatic patients, that featured a nonuniversal colonoscopy design, that included only 2 of the 3 comparison groups, and that had fewer than 300 participants received 0 points for each category (for a minimum score of 0). Studies with low scores (0, 1, 2, or 3) were compared with studies with high scores (4 or 5). Because this meta-analysis included only published studies, we explored the possibility of publication bias by performing an inverted funnel plot analysis.

STUDY SELECTION

On preliminary review of the titles and abstracts of citations found by our search algorithm, 52 potentially pertinent studies were identified. Subsequently, the full text of each study was reviewed, and 31 were excluded: 13 because they reported the prevalence of PN in patients with distal TAs but not distal HPs,1426 4 because they presented distal findings in patients stratified by proximal findings instead of vice versa,2730 6 because subsequent follow-up findings were reported instead of concurrent proximal findings,3136 1 because it reported the risk of neoplasia anywhere in the colon in patients with distal HPs,37 1 because it compared patients with distal HPs with patients with “any” distal polyp,38 1 because it provided data on patients with distal HPs with or without distal TAs,39 4 because they did not present polyp findings stratified by location or histologic features,4043 and, last, 1 because it did not report actual numbers of patients, although it concluded that distal HPs were not markers for PN because of a nonsignificant RR of 1.2.44

Twenty-one studies4565 met the inclusion criteria, representing a total of 20 402 participants. Characteristics of the included studies are described in Table 1. Of these studies, 3 compared the prevalence of PN in patients with distal HPs vs those with no distal polyps,47,55,56 8 compared the prevalence of PN in patients with distal HPs vs those with distal TAs,45,49,53,54,58,60,61,65 and the remaining 10 included both comparisons.46,48,5052,57,59,6264 Nine studies imposed age restrictions on eligible participants (either ≥50 or ≥40 years). Six studies excluded individuals with a family history of CRC. Four studies restricted participants to those with only diminutive distal polyps (≤5 mm). Two studies reported results for PAN only,49,61 and 2 reported results for PAN and PN.59,62 Three studies5961 were published in abstract form only.

Table Graphic Jump LocationTable 1. Characteristics of Included Studies in Chronological Order
DATA ANALYSIS

Of 20 402 individuals included in this analysis, 11 367 had no distal polyps, 4216 had distal HPs only, and 4819 had at least 1 distal TA. In 12 of the included studies,4547,49,50,54,55,58,60,61,63,66 the investigators concluded that distal HPs were markers for PN because the prevalence of PN in those with distal HPs was either similar to that in patients with distal TAs or significantly higher than that in patients with no distal polyps; the remaining 9 studies48,5153,56,57,59,62,65 concluded that distal HPs were not markers (Table 2).

Table Graphic Jump LocationTable 2. Data From the Included Studies in Chronological Order*

Figure 1A describes the 11 studies that compared the prevalence of PN in patients with distal HPs vs those with no distal polyps.Using the DerSimonian and Laird method based on a random-effects model, the summary RR was 1.81 (95% CI, 1.20-2.73), indicating an elevated risk of PN in patients with distal HPs vs those with no distal polyps. There was significant heterogeneity (Q = 84.7; P < .001). The summary prevalence of PN was 25.97% (95% CI, 23.95%-27.98%) in the distal HP group. Figure 1B describes the 16 studies that compared the prevalence of PN in patients with distal TAs vs those with distal HPs. The summary RR was 0.69 (95% CI, 0.60-0.80), showing a reduced risk of PN in patients with distal HPs vs those with distal TAs. There was borderline heterogeneity (Q = 22.9; P = .08).

Place holder to copy figure label and caption
Figure 1.

Forrest plots of studies comparing the prevalence of proximal neoplasia in patients with distal hyperplastic polyps vs those with no distal polyps (A) or those with distal tubular adenomas (B). The no distal polyp group and the distal tubular adenoma group are assumed to have a risk of 1.0. A high risk ratio implies that distal hyperplastic polyps are associated with more risk of proximal neoplasia. CI indicates confidence interval.

Graphic Jump Location

Four studies reported data on PAN (Figure 2). For patients with distal HP vs those with no distal polyps, the summary RR was 1.02 (95% CI, 0.62-1.68), with borderline heterogeneity (Q = 4.74; P = .09). For patients with distal HPs vs those with distal TAs, the summary RR was 0.52 (95% CI, 0.32-0.84), again with borderline heterogeneity (Q = 8.1; P = .04). The summary prevalence of PAN was 4.41% (95% CI, 3.87%-4.96%) in individuals with distal HPs. One study52 reported results using 2 different definitions of the demarcation between the proximal and distal colon; this did not statistically significantly affect the results.

Place holder to copy figure label and caption
Figure 2.

Forrest plots of studies comparing the prevalence of proximal advanced neoplasia in patients with distal hyperplastic polyps vs those with no distal polyps (A) or those with distal tubular adenomas (B). The no distal polyp group and the distal tubular adenoma group are assumed to have a risk of 1.0. A high risk ratio implies that distal hyperplastic polyps are associated with more risk of proximal advanced neoplasia. CI indicates confidence interval.

Graphic Jump Location
SUBGROUP AND SENSITIVITY ANALYSIS

Comparing the risk of PN in patients with distal HP vs those with no distal polyps, the inverse variance and Mantel-Haenszel methods (both based on a fixed-effects model) gave summary RRs of 1.17 (95% CI, 1.06-1.29) and 1.08 (95% CI, 0.98-1.19), respectively. For patients with distal HPs vs those with distal TAs, the inverse variance and Mantel-Haenszel methods gave summary RRs of 0.68 (95% CI, 0.62-0.74) and 0.66 (95% CI, 0.61-0.72), respectively.

Stratification by study design, publication date, demarcation definition, and restrictions on age, family history of CRC, and distal polyp size resulted in no clinically significant changes in the results (data not shown). Stratification by sample size showed a trend toward a higher risk of PN in smaller studies. The RR for PN was 1.03 in large studies vs 1.88 in small studies when the distal HP group was compared with the no distal polyp group, but the 95% CIs overlapped.

Because the test for heterogeneity is known to have low sensitivity and all our Q statistic values are either high or borderline, in the rest of this article we report only the results based on the DerSimonian and Laird method (random-effects model). Not only is this approach more conservative (ie, usually associated with wider CIs), but it is also more appropriate considering the heterogeneity present and will tend to lessen the impact of the 4 studies with extremely large sample sizes.

Figure 3 shows the summary RRs stratified by patient symptoms.For screening studies, the risk of PN in the distal HP group was statistically similar to that of the no distal polyp group (RR = 1.25; 95% CI, 0.92-1.70) but lower than that of the distal TA group (RR = 0.65; 95% CI, 0.55-0.76), whereas the opposite was true for diagnostic studies (RR = 2.95; 95% CI, 1.40-6.21 and RR = 0.85; 95% CI, 0.69-1.04, respectively).When studies were stratified by quality scores, in those with high scores, the risk of PN in the distal HP group was similar to that in the no distal polyp group (RR = 1.18; 95% CI, 0.88-1.59) but lower than that in the distal TA group (RR = 0.60; 95% CI, 0.50-0.70); again, the opposite was true for studies with low quality scores.

Place holder to copy figure label and caption
Figure 3.

Subgroup analyses of studies comparing the prevalence of proximal neoplasia in patients with distal hyperplastic polyps vs those with no distal polyps (A) or those with distal tubular adenomas (B), stratified by patient symptoms. The no distal polyp group and the distal adenoma group are assumed to have a risk of 1.0. A high risk ratio implies that distal hyperplastic polyps are associated with more risk of proximal neoplasia. CI indicates confidence interval.

Graphic Jump Location

To test whether any study had a dominant effect, we excluded each study in turn and recalculated the summary RR.64 We did not find a dominant study. To assess the impact of possible publication bias, we constructed an inverted funnel plot (data not shown). This figure exhibited asymmetry, suggesting publication bias, but the effect did not seem to be severe because the plot could be made symmetrical by eliminating 2 to 3 studies at the edge of the funnel.

In current practice, there are various approaches to dealing with small polyps found by FS.67 Two previous meta-analyses68,69 of the clinical significance of distal HPs have been published. One meta-analysis68 summarized the results of 18 studies, including 3 reported only in abstract form. Using a random-effects model, the researchers concluded that distal HPs were associated with a prevalence of 21% to 25% for PN and 4% to 5% for PAN and “may justify examination of the proximal colon.” The summary RR was nonsignificant at 1.3 (95% CI, 0.9-1.8) for PN but significant at 2.6 (95% CI, 1.1-5.9) for PAN (based on only 2 studies). Like our study, it showed a difference in results when the data were stratified according to patient symptoms. However, this meta-analysis did not include results from 3 studies that were included in our review55,59,62 and included 1 study that we excluded owing to lack of a control group.38 The other meta-analysis69 included only 6 studies and concluded that distal HPs were not associated with PN, with a summary RR of 1.44 (95% CI, 0.79-2.62).

In our meta-analysis, for individuals with distal HPs, the overall prevalence was approximately 26% for PN and 4.4% for PAN. The overall RR for PN in the distal HP group was intermediate between the no distal polyp group and the distal TAgroup. However, the observational studies included in our meta-analysis are heterogeneous; therefore, subgroup analysis is important and is discussed in the following subsection.

STRATIFICATION ACCORDING TO PATIENT SYMPTOMS

Compared with screening procedures, diagnostic colonoscopies on symptomatic patients are probably more likely to uncover neoplasia in the proximal and distal colon. Because the significance of distal HPs is relevant mainly to asymptomatic individuals, screening studies are more likely to give a valid answer to our study question. If we stratify the data according to whether diagnostic or screening procedures were performed, we find that only 6 of 14 screening studies45,46,48,5054,57,59,61,62,65,66 concluded that HPs were markers for PN, in contrast to 6 of 7 studies on symptomatic patients.47,49,55,56,58,60,63 When we stratified the studies by patient symptoms, heterogeneity was eliminated for screening studies (Q = 12.3) but not for diagnostic studies (Q = 22.3). As expected, the mean prevalence of PN in patients with distal HPs is higher in diagnostic studies than in screening studies (approximately 32% vs 23%), but it is unclear why the relative risk in the distal HP group (compared with the other 2 groups) should also be higher in diagnostic studies.

STRATIFICATION ACCORDING TO STUDY QUALITY

Studies with higher quality scores tended to show that distal HPs were not markers for PN. This can be understood if we consider how study quality was defined in our review. Aside from being restricted to screening individuals and using a universal colonoscopy design, high-quality studies were more likely to include large numbers of individuals in each of the 3 comparison groups. In contrast, low-quality studies tended to be small studies that compared the prevalence of PN in patients with distal HPs with either those with distal TAs or those with no distal polyps. Studies that report only the former comparison may have inadequate statistical power, leading to a type II error. On the other hand, studies that report only the latter may demonstrate that the risk in the distal HP group is significantly higher than that in the no distal polyp group but may not show whether that risk is comparable with that in the distal TA group. The largest study62 in our meta-analysis (with 7250 patients) did not have a true control group. Instead, the “no distal polyp” group consisted of patients with no distal polyps found on follow-up colonoscopy or distal “polyps” found to consist of normal tissue when biopsied during colonoscopy; this can potentially bias the results.

SENSITIVITY ANALYSIS ACCORDING TO META-ANALYTIC TECHNIQUE

The RR for PN in the distal HP group vs the no distal polyp group is higher when random-effects methods are used as opposed to fixed-effects methods (1.81 vs 1.17). The DerSimonian and Laird method, a random-effects method, is usually more conservative than fixed-effects methods. This usually means that the 95% CI of the summary effect size is wider, especially in the presence of large between-study heterogeneity because the random-effects model incorporates a between-study component of variance. However, the DerSimonian and Laird method can sometimes result in a larger summary effect size estimate because it gives more weight to small studies than fixed-effects methods. As the between-study variance becomes large (ie, when there is heterogeneity), the between-study variance comes to dominate the weights assigned to each study, and large and small studies will tend to be weighted almost equally.70,71 In our meta-analysis, the summary effect size is larger using random-effects models because the smaller studies tend to report larger effect sizes than the larger ones (although the difference was not statistically significant), possibly owing to subtle publication bias. Specifically, when we compared the distal HP group with the no distal polyp group, the summary RRs were different with the 3 different techniques, which is consistent with the high degree of heterogeneity (Q = 84.7). In contrast, when we compared the distal HP group with the distal TA group, the summary RRs were similar using the 3 techniques because the degree of heterogeneity was low (Q = 22.9).

Despite our efforts, there are several limitations to this study. Publication bias is a concern in all meta-analyses because it is well known that studies with null results are less likely to be published. This may explain the large number of “positive” studies that reported an increased risk of PN in patients with distal HPs. In particular, 5 of these “positive” studies45,54,58,60,61 were small and compared only the distal HP group with the distal TA group, making them highly susceptible to a type II error owing to lack of statistical power; it is probably no coincidence that 2 of these studies were reported in abstract form only. Our inverted funnel plot analysis indicates that publication bias may be present but is unlikely to be highly significant.

Most studies in this review look at the relationship between distal findings and PN (ie, adenomas). Many of these proximal adenomas were small (<5 mm); therefore, their clinical significance is uncertain. Small adenomas are still neoplastic and may be precancerous, but some studies32,72 suggest that they are not associated with any increased risk of CRC.

Despite the large number of patients in this meta-analysis, the number of those with PAN is relatively small. This is the most likely reason for the lack of statistical significance when we compared the prevalence of PAN among the 3 groups, although there seems to be a trend toward a higher risk of PAN in patients with distal TA vs the other 2 groups.

The results of this study are important in determining whether individuals initially screened by FS should be referred for colonoscopy. Although some guidelines4 consider colonoscopic screening of all individuals 50 years and older to be a “preferred” strategy, others1,3 regard screening by FS every 5 years (with annual fecal occult blood testing) to be as acceptable as colonoscopy every 10 years. At present, only approximately 30% of age-eligible persons undergo any type of endoscopic screening in the United States.73 Attempts to implement universal colonoscopic screening are affected by a variety of factors, including cost-effectiveness, patient acceptance, insurance coverage, and availability of adequately trained colonoscopists. Thus, it is likely that FS will continue to play an important role in CRC screening.

Although the overall summary RR of PN is elevated in patients with distal HPs vs those with no distal polyps, subgroup analysis demonstrates that studies that are more likely to provide valid answers to our study question show that distal HPs are not associated with an increased risk of PN. Specifically, studies that involve only asymptomatic screening individuals and are judged to have higher quality based on our scoring system show that the prevalence of PN in the distal HP group is similar to that in the no distal polyp group and lower than that in the distal TA group. The absence of an association between distal HPs and PN support current screening guidelines that recommend against the use of colonoscopic follow-up for patients with only HPs identified by screening FS. Currently, biopsies are often not performed during screening FS, with many practitioners automatically referring for colonoscopy all patients found to have distal polyps. This study illustrates that it is important for practitioners to biopsy distal polyps because some patients will be found to have distal HPs and may not require colonoscopy.

Correspondence: Otto S. Lin, MD, MSc, C3-Gas, Gastroenterology Section, Virginia Mason Medical Center, 1100 Ninth Ave, Seattle, WA 98101 (Otto.Lin@vmmc.org).

Accepted for Publication: October 11, 2004.

Financial Disclosure: None.

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Dinning  JPHixson  LJClark  LC Prevalence of distal colonic neoplasia associated with proximal colon cancers. Arch Intern Med 1994;154853- 856
PubMed Link to Article
Castiglione  GCiatto  SMazzotta  AGrazzini  G Sensitivity of screening sigmoidoscopy for proximal colorectal tumours. Lancet 1995;345726- 727
PubMed Link to Article
Huang  EHWhelan  RLGleason  NR  et al.  Increased incidence of colorectal adenomas in follow-up evaluation of patients with newly diagnosed hyperplastic polyps. Surg Endosc 2001;15646- 648
PubMed Link to Article
Atkin  WSMorson  BCCuzick  J Long-term risk of colorectal cancer after excision of rectosigmoid adenomas. N Engl J Med 1992;326658- 662
PubMed Link to Article
Spencer  RJMelton  LJ  IIIReady  RLIlstrup  DM Treatment of small colorectal polyps: a population-based study of the risk of subsequent carcinoma. Mayo Clin Proc 1984;59305- 310
PubMed Link to Article
Ellis  CNBoggs  HWSlagle  CWCole  PACoyle  DJ Incidence of metachronous adenomatous polyps in patients with hyperplastic polyps [abstract]. Gastrointest Endosc 1991;37262
Bensen  SPCole  BFMott  LABaron  JASandler  RSHaile  R Colorectal hyperplastic polyps and risk of recurrence of adenomas and hyperplastic polyps: Polyps Prevention Study. Lancet 1999;3541873- 1874
PubMed Link to Article
Liljegren  ALindblom  ARotstein  SNilsson  BRubio  CJaramillo  E Prevalence and incidence of hyperplastic polyps and adenomas in familial colorectal cancer: correlation between the two types of colon polyps. Gut 2003;521140- 1147
PubMed Link to Article
Khvatyuk  OZaubert  AGWinawer  SJ Association of hyperplastic polyps and advanced adenomas: are there high risk hyperplastic polyps [abstract]? Am J Gastroenterol 2001;96S154
Link to Article
Olsen  HWLawrence  WA Hyperplastic polyps at screening sigmoidoscopy are not an indication for colonoscopy [abstract]. Gastrointest Endosc 1998;47312
Sciallero  SCostantini  MBertinelli  E  et al.  Distal hyperplastic polyps do not predict proximal adenomas: results from a multicentric study of colorectal adenomas. Gastrointest Endosc 1997;46124- 130
PubMed Link to Article
Betes  MMunoz-Navas  MADuque  JM  et al.  Use of colonoscopy as a primary screening test for colorectal cancer in average risk people. Am J Gastroenterol 2003;982648- 2654
PubMed
Weston  APCampbell  DR Diminutive colonic polyps: histopathology, spatial distribution, concomitant significant lesions, and treatment complications. Am J Gastroenterol 1995;9024- 28
PubMed
Pines  ABat  LRosenbaum  JLevo  YShemesh  E Are tiny polyps important when found on sigmoidoscopy in asymptomatic people? J Clin Gastroenterol 1992;15113- 116
PubMed Link to Article
Matter  SECampbell  DR Significance of distal polyps detected with flexible sigmoidoscopy in asymptomatic patients. Arch Intern Med 1992;1521776- 1780
PubMed Link to Article
Zauber  AWinawer  SBiaz  B  et al.  The National Polyp Study (NPS): the association of colonic hyperplastic polyps and adenomas [abstract]. Am J Gastroenterol 1988;831060
Blue  MGSivak  MV  JrAchkar  EMatzen  RStahl  RR Hyperplastic polyps seen at sigmoidoscopy are markers for additional adenomas seen at colonoscopy. Gastroenterology 1991;100564- 566
PubMed
Achkar  ECarey  W Small polyps found during fiberoptic sigmoidoscopy in asymptomatic patients. Ann Intern Med 1988;109880- 883
PubMed Link to Article
Ansher  AFLewis  JHFleischer  DE  et al.  Hyperplastic colonic polyps as a marker for adenomatous colonic polyps. Am J Gastroenterol 1989;84113- 117
PubMed
Brady  PGStraker  RJMcClave  SANord  HJPinkas  MRobinson  BE Are hyperplastic rectosigmoid polyps associated with an increased risk of proximal colonic neoplasms? Gastrointest Endosc 1993;39481- 485
PubMed Link to Article
Ellis  CNBoggs  HWSlagle  GWCole  PACoyle  DJ Clinical significance of diminutive polyps of the rectum and sigmoid colon. Dis Colon Rectum 1993;368- 9
PubMed Link to Article
Foutch  PGDiSario  JAPardy  KMai  HDManne  RK The sentinel hyperplastic polyp: a marker for synchronous neoplasia in the proximal colon. Am J Gastroenterol 1991;861482- 1485
PubMed
Lieberman  DASmith  FW Screening for colon malignancy with colonoscopy. Am J Gastroenterol 1991;86946- 951
PubMed
Lieberman  DAWeiss  DGBond  JHAhnen  DJGarewal  HChejfec  G Use of colonoscopy to screen asymptomatic adults for colorectal cancer: Veterans Affairs Cooperative Study Group 380. N Engl J Med 2000;343162- 168
PubMed Link to Article
Nusko  GAltendorf-Hofmann  AHermanek  PEll  CHahn  EG Correlation of polypoid lesions in the distal colorectum and proximal colon in asymptomatic screening subjects. Eur J Gastroenterol Hepatol 1996;8351- 354
PubMed Link to Article
Opelka  FGTimmcke  AEGathright  JB  JrRay  JEHicks  TC Diminutive colonic polyps: an indication for colonoscopy. Dis Colon Rectum 1992;35178- 181
PubMed Link to Article
Provenzale  DMartin  ZZHolland  KLSandler  RS Colon adenomas in patients with hyperplastic polyps. J Clin Gastroenterol 1988;1046- 49
PubMed Link to Article
Provenzale  DGarrett  JWCondon  SESandler  RS Risk for colon adenomas in patients with rectosigmoid hyperplastic polyps. Ann Intern Med 1990;113760- 763
PubMed Link to Article
Rex  DKSmith  JJUlbright  TMLehman  GA Distal colonic hyperplastic polyps do not predict proximal adenomas in asymptomatic average-risk subjects. Gastroenterology 1992;102317- 319
PubMed
Rokkas  TKarameris  AMikou  G Small polyps found at sigmoidoscopy: are they significant? Hepatogastroenterology 1993;40475- 477
PubMed
Lin  OSFrance  RSchembre  DBKozarek  RA Risk of proximal colorectal neoplasia in patients with distal hyperplastic polyps [abstract]. Am J Gastroenterol 2003;98S109
Link to Article
Stoltenberg  PHKirtley  DW Are diminutive colorectal polyps clinically significant [abstract]? Gastrointest Endosc 1988;34172
Deal  SEWoogen  SDStuckey  CZfass  AM Screening sigmoidoscopy for colonic neoplasms: hyperplastic polyps require further evaluation and 30 cm flexible sigmoidoscopy is inadequate [abstract]. Gastrointest Endosc 1991;37262
Pinsky  PFSchoen  REWeissfeld  JLBresalier  RSHayes  RBGohagan  JK Predictors of advanced proximal neoplasia in persons with abnormal screening flexible sigmoidoscopy. Clin Gastroenterol Hepatol 2003;1103- 110
PubMed Link to Article
Pennazio  MArrigoni  ARisio  MSpandre  MRossini  FP Small rectosigmoid polyps as markers of proximal neoplasms. Dis Colon Rectum 1993;361121- 1125
PubMed Link to Article
Imperiale  TFWagner  DRLin  CYLarkin  GNRogge  JDRansohoff  DF Using risk for advanced proximal colonic neoplasia to tailor endoscopic screening for colorectal cancer. Ann Intern Med 2003;139959- 965
PubMed Link to Article
Ullah  NQureshi  KHatfield  J  et al.  Small early tubular adenomas and mixed colonic polyps found on screening flexible sigmoidoscopy do not predict proximal neoplasia in males. Clin Gastroenterol Hepatol 2004;2246- 251
PubMed Link to Article
Imperiale  TFWagner  DRLin  CYLarkin  GNRogge  JDRansohoff  DF Risk of advanced proximal neoplasms in asymptomatic adults according to the distal colorectal findings. N Engl J Med 2000;343169- 174
PubMed Link to Article
Rex  DK The small polyp at flexible sigmoidoscopy: an historical perspective on why practices still vary. J Clin Gastroenterol 1999;2819- 22
PubMed Link to Article
Dave  SHui  SKroenke  KImperiale  TF Is the distal hyperplastic polyp a marker for proximal neoplasia? J Gen Intern Med 2003;18128- 137
PubMed Link to Article
Lewis  JDNg  KHung  KE  et al.  Detection of proximal adenomatous polyps with screening sigmoidoscopy: a systematic review and meta-analysis of screening colonoscopy. Arch Intern Med 2003;163413- 420
PubMed Link to Article
Egger  MSmith  GDAltman  DG Systematic Reviews in Health Care: Meta-analysis in Context. 2nd ed. London, England BMJ Books2001;
Petitti  DB Meta-analysis, Decision Analysis and Cost-effectiveness Analysis. 2nd ed. New York, NY Oxford University Press2000;
Hofstad  BVatn  MHAndersen  SN  et al.  Growth of colorectal polyps: redetection and evaluation of unresected polyps for a period of three years. Gut 1996;39449- 456
PubMed Link to Article
Lemon  SZapka  JPuleo  ELuckmann  RChasan-Taber  L Colorectal cancer screening participation: comparisons with mammography and prostate-specific antigen screening. Am J Public Health 2001;911264- 1272
PubMed Link to Article
Sutton  AJAbrams  KRJones  DRSheldon  TASong  F Methods for Meta-analysis in Medical Research.  New York, NY John Wiley & Sons2000;

Figures

Place holder to copy figure label and caption
Figure 1.

Forrest plots of studies comparing the prevalence of proximal neoplasia in patients with distal hyperplastic polyps vs those with no distal polyps (A) or those with distal tubular adenomas (B). The no distal polyp group and the distal tubular adenoma group are assumed to have a risk of 1.0. A high risk ratio implies that distal hyperplastic polyps are associated with more risk of proximal neoplasia. CI indicates confidence interval.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 2.

Forrest plots of studies comparing the prevalence of proximal advanced neoplasia in patients with distal hyperplastic polyps vs those with no distal polyps (A) or those with distal tubular adenomas (B). The no distal polyp group and the distal tubular adenoma group are assumed to have a risk of 1.0. A high risk ratio implies that distal hyperplastic polyps are associated with more risk of proximal advanced neoplasia. CI indicates confidence interval.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 3.

Subgroup analyses of studies comparing the prevalence of proximal neoplasia in patients with distal hyperplastic polyps vs those with no distal polyps (A) or those with distal tubular adenomas (B), stratified by patient symptoms. The no distal polyp group and the distal adenoma group are assumed to have a risk of 1.0. A high risk ratio implies that distal hyperplastic polyps are associated with more risk of proximal neoplasia. CI indicates confidence interval.

Graphic Jump Location

Tables

Table Graphic Jump LocationTable 1. Characteristics of Included Studies in Chronological Order
Table Graphic Jump LocationTable 2. Data From the Included Studies in Chronological Order*

References

Smith  RAvon Eschenbach  ACWender  R  et al.  American Cancer Society guidelines for the early detection of cancer: update of early detection guidelines for prostate, colorectal, and endometrial cancers. CA Cancer J Clin 2001;5138- 75
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Bond  JHPractice Parameters Committee of the American College of Gastroenterology, Polyp guideline: diagnosis, treatment, and surveillance for patients with colorectal polyps. Am J Gastroenterol 2000;953053- 3063
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Winawer  SFletcher  RRex  D  et al.  Colorectal cancer screening and surveillance: clinical guidelines and rationale: update based on new evidence. Gastroenterology 2003;124544- 560
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Rex  DKJohnson  DALieberman  DABurt  RWSonnenberg  A Colorectal cancer prevention 2000: screening recommendations of the American College of Gastroenterology. Am J Gastroenterol 2000;95868- 877
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Hawkins  NJWard  RL Sporadic colorectal cancers with microsatellite instability and their possible origin in hyperplastic polyps and serrated adenomas. J Natl Cancer Inst 2001;931307- 1313
PubMed Link to Article
Otori  KOda  YSugiyama  K  et al.  High frequency of K-ras mutations in human colorectal hyperplastic polyps. Gut 1997;40660- 663
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Jass  JR Hyperplastic polyps and colorectal cancer: is there a link? Clin Gastroenterol Hepatol 2004;21- 8
PubMed Link to Article
Martinez  MEMcPherson  RSLevin  BGlober  GA A case-control study of dietary intake and other lifestyle risk factors for hyperplastic polyps. Gastroenterology 1997;113423- 429
PubMed Link to Article
Kearney  JGiovannucci  ERimm  EB  et al.  Diet, alcohol, and smoking and the occurrence of hyperplastic polyps of the colon and rectum (United States). Cancer Causes Control 1995;645- 56
PubMed Link to Article
Yamada  Ted Textbook of Gastroenterology. 4th ed. Philadelphia, Pa Lippincott Williams & Wilkins2003;
Feldman  Med Sleisenger and Fordtran's Gastrointestinal and Liver Disease. 7th ed. Philadelphia, Pa WB Saunders Co2002;
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Friedenreich  CM Methods for pooled analyses of epidemiologic studies. Epidemiology 1993;4295- 302
PubMed Link to Article
McGarrity  TJBhatti  AMPeters  DJPeiffer  LPKumar  AInverso  N Synchronous proximal polyps and cancer in patients with polyps detected at sigmoidoscopy: results of a single, rural-based sigmoidoscopy clinic. Dig Dis Sci 2002;47309- 316
PubMed Link to Article
Kadakia  SCWrobleski  CSKadakia  ASMeier  NJ Prevalence of proximal colonic polyps in average-risk asymptomatic patients with negative fecal occult blood tests and flexible sigmoidoscopy. Gastrointest Endosc 1996;44112- 117
PubMed Link to Article
Levin  TRPalitz  AGrossman  S  et al.  Predicting advanced proximal colonic neoplasia with screening sigmoidoscopy. JAMA 1999;2811611- 1617
PubMed Link to Article
Wallace  MBKemp  JATrnka  YMDonovan  JMFarraye  FA Is colonoscopy indicated for small adenomas found by screening flexible sigmoidoscopy? Ann Intern Med 1998;129273- 278
PubMed Link to Article
Read  TERead  JDButterly  LF Importance of adenomas 5 mm or less in diameter that are detected by sigmoidoscopy. N Engl J Med 1997;3368- 12
PubMed Link to Article
Zarchy  TMErshoff  D Do characteristics of adenomas on flexible sigmoidoscopy predict advanced lesions on baseline colonoscopy? Gastroenterology 1994;1061501- 1504
PubMed
Nicholson  FBKorman  MGStern  AIHansky  J Distribution of colorectal adenomas: implications for bowel cancer screening. Med J Aust 2000;172428- 430
PubMed
Johnson  DAGurney  MSVolpe  RJ  et al.  A prospective study of the prevalence of colonic neoplasms in asymptomatic patients with an age-related risk. Am J Gastroenterol 1990;85969- 974
PubMed
Rex  DKLehman  GAHawes  RHUlbright  TMSmith  JJ Screening colonoscopy in asymptomatic average-risk persons with negative fecal occult blood tests. Gastroenterology 1991;10064- 67
PubMed
McConnell  JCNizin  JSSlade  MS Colonoscopy in patients with a primary family history of colon cancer. Dis Colon Rectum 1990;33105- 107
PubMed Link to Article
Sciallero  SBonelli  LAste  H  et al.  Do patients with rectosigmoid adenomas 5 mm or less in diameter need total colonoscopy? Gastrointest Endosc 1999;50314- 321
PubMed Link to Article
Ryan  MENorfleet  RGKirchner  JP  et al.  The significance of diminutive colonic polyps found at flexible sigmoidoscopy. Gastrointest Endosc 1989;3585- 89
PubMed Link to Article
Collett  JAPlatell  CFletcher  DRAquilia  SOlynyk  JK Distal colonic neoplasms predict proximal neoplasia in average-risk, asymptomatic subjects. J Gastroenterol Hepatol 1999;1467- 71
PubMed Link to Article
Foutch  PGMai  HPardy  KDiSario  JAManne  RKKerr  D Flexible sigmoidoscopy may be ineffective for secondary prevention of colorectal cancer in asymptomatic, average-risk men. Dig Dis Sci 1991;36924- 928
PubMed Link to Article
Lemmel  GTHaseman  JHRex  DKRahmani  E Neoplasia distal to the splenic flexure in patients with proximal colon cancer. Gastrointest Endosc 1996;44109- 111
PubMed Link to Article
Dinning  JPHixson  LJClark  LC Prevalence of distal colonic neoplasia associated with proximal colon cancers. Arch Intern Med 1994;154853- 856
PubMed Link to Article
Castiglione  GCiatto  SMazzotta  AGrazzini  G Sensitivity of screening sigmoidoscopy for proximal colorectal tumours. Lancet 1995;345726- 727
PubMed Link to Article
Huang  EHWhelan  RLGleason  NR  et al.  Increased incidence of colorectal adenomas in follow-up evaluation of patients with newly diagnosed hyperplastic polyps. Surg Endosc 2001;15646- 648
PubMed Link to Article
Atkin  WSMorson  BCCuzick  J Long-term risk of colorectal cancer after excision of rectosigmoid adenomas. N Engl J Med 1992;326658- 662
PubMed Link to Article
Spencer  RJMelton  LJ  IIIReady  RLIlstrup  DM Treatment of small colorectal polyps: a population-based study of the risk of subsequent carcinoma. Mayo Clin Proc 1984;59305- 310
PubMed Link to Article
Ellis  CNBoggs  HWSlagle  CWCole  PACoyle  DJ Incidence of metachronous adenomatous polyps in patients with hyperplastic polyps [abstract]. Gastrointest Endosc 1991;37262
Bensen  SPCole  BFMott  LABaron  JASandler  RSHaile  R Colorectal hyperplastic polyps and risk of recurrence of adenomas and hyperplastic polyps: Polyps Prevention Study. Lancet 1999;3541873- 1874
PubMed Link to Article
Liljegren  ALindblom  ARotstein  SNilsson  BRubio  CJaramillo  E Prevalence and incidence of hyperplastic polyps and adenomas in familial colorectal cancer: correlation between the two types of colon polyps. Gut 2003;521140- 1147
PubMed Link to Article
Khvatyuk  OZaubert  AGWinawer  SJ Association of hyperplastic polyps and advanced adenomas: are there high risk hyperplastic polyps [abstract]? Am J Gastroenterol 2001;96S154
Link to Article
Olsen  HWLawrence  WA Hyperplastic polyps at screening sigmoidoscopy are not an indication for colonoscopy [abstract]. Gastrointest Endosc 1998;47312
Sciallero  SCostantini  MBertinelli  E  et al.  Distal hyperplastic polyps do not predict proximal adenomas: results from a multicentric study of colorectal adenomas. Gastrointest Endosc 1997;46124- 130
PubMed Link to Article
Betes  MMunoz-Navas  MADuque  JM  et al.  Use of colonoscopy as a primary screening test for colorectal cancer in average risk people. Am J Gastroenterol 2003;982648- 2654
PubMed
Weston  APCampbell  DR Diminutive colonic polyps: histopathology, spatial distribution, concomitant significant lesions, and treatment complications. Am J Gastroenterol 1995;9024- 28
PubMed
Pines  ABat  LRosenbaum  JLevo  YShemesh  E Are tiny polyps important when found on sigmoidoscopy in asymptomatic people? J Clin Gastroenterol 1992;15113- 116
PubMed Link to Article
Matter  SECampbell  DR Significance of distal polyps detected with flexible sigmoidoscopy in asymptomatic patients. Arch Intern Med 1992;1521776- 1780
PubMed Link to Article
Zauber  AWinawer  SBiaz  B  et al.  The National Polyp Study (NPS): the association of colonic hyperplastic polyps and adenomas [abstract]. Am J Gastroenterol 1988;831060
Blue  MGSivak  MV  JrAchkar  EMatzen  RStahl  RR Hyperplastic polyps seen at sigmoidoscopy are markers for additional adenomas seen at colonoscopy. Gastroenterology 1991;100564- 566
PubMed
Achkar  ECarey  W Small polyps found during fiberoptic sigmoidoscopy in asymptomatic patients. Ann Intern Med 1988;109880- 883
PubMed Link to Article
Ansher  AFLewis  JHFleischer  DE  et al.  Hyperplastic colonic polyps as a marker for adenomatous colonic polyps. Am J Gastroenterol 1989;84113- 117
PubMed
Brady  PGStraker  RJMcClave  SANord  HJPinkas  MRobinson  BE Are hyperplastic rectosigmoid polyps associated with an increased risk of proximal colonic neoplasms? Gastrointest Endosc 1993;39481- 485
PubMed Link to Article
Ellis  CNBoggs  HWSlagle  GWCole  PACoyle  DJ Clinical significance of diminutive polyps of the rectum and sigmoid colon. Dis Colon Rectum 1993;368- 9
PubMed Link to Article
Foutch  PGDiSario  JAPardy  KMai  HDManne  RK The sentinel hyperplastic polyp: a marker for synchronous neoplasia in the proximal colon. Am J Gastroenterol 1991;861482- 1485
PubMed
Lieberman  DASmith  FW Screening for colon malignancy with colonoscopy. Am J Gastroenterol 1991;86946- 951
PubMed
Lieberman  DAWeiss  DGBond  JHAhnen  DJGarewal  HChejfec  G Use of colonoscopy to screen asymptomatic adults for colorectal cancer: Veterans Affairs Cooperative Study Group 380. N Engl J Med 2000;343162- 168
PubMed Link to Article
Nusko  GAltendorf-Hofmann  AHermanek  PEll  CHahn  EG Correlation of polypoid lesions in the distal colorectum and proximal colon in asymptomatic screening subjects. Eur J Gastroenterol Hepatol 1996;8351- 354
PubMed Link to Article
Opelka  FGTimmcke  AEGathright  JB  JrRay  JEHicks  TC Diminutive colonic polyps: an indication for colonoscopy. Dis Colon Rectum 1992;35178- 181
PubMed Link to Article
Provenzale  DMartin  ZZHolland  KLSandler  RS Colon adenomas in patients with hyperplastic polyps. J Clin Gastroenterol 1988;1046- 49
PubMed Link to Article
Provenzale  DGarrett  JWCondon  SESandler  RS Risk for colon adenomas in patients with rectosigmoid hyperplastic polyps. Ann Intern Med 1990;113760- 763
PubMed Link to Article
Rex  DKSmith  JJUlbright  TMLehman  GA Distal colonic hyperplastic polyps do not predict proximal adenomas in asymptomatic average-risk subjects. Gastroenterology 1992;102317- 319
PubMed
Rokkas  TKarameris  AMikou  G Small polyps found at sigmoidoscopy: are they significant? Hepatogastroenterology 1993;40475- 477
PubMed
Lin  OSFrance  RSchembre  DBKozarek  RA Risk of proximal colorectal neoplasia in patients with distal hyperplastic polyps [abstract]. Am J Gastroenterol 2003;98S109
Link to Article
Stoltenberg  PHKirtley  DW Are diminutive colorectal polyps clinically significant [abstract]? Gastrointest Endosc 1988;34172
Deal  SEWoogen  SDStuckey  CZfass  AM Screening sigmoidoscopy for colonic neoplasms: hyperplastic polyps require further evaluation and 30 cm flexible sigmoidoscopy is inadequate [abstract]. Gastrointest Endosc 1991;37262
Pinsky  PFSchoen  REWeissfeld  JLBresalier  RSHayes  RBGohagan  JK Predictors of advanced proximal neoplasia in persons with abnormal screening flexible sigmoidoscopy. Clin Gastroenterol Hepatol 2003;1103- 110
PubMed Link to Article
Pennazio  MArrigoni  ARisio  MSpandre  MRossini  FP Small rectosigmoid polyps as markers of proximal neoplasms. Dis Colon Rectum 1993;361121- 1125
PubMed Link to Article
Imperiale  TFWagner  DRLin  CYLarkin  GNRogge  JDRansohoff  DF Using risk for advanced proximal colonic neoplasia to tailor endoscopic screening for colorectal cancer. Ann Intern Med 2003;139959- 965
PubMed Link to Article
Ullah  NQureshi  KHatfield  J  et al.  Small early tubular adenomas and mixed colonic polyps found on screening flexible sigmoidoscopy do not predict proximal neoplasia in males. Clin Gastroenterol Hepatol 2004;2246- 251
PubMed Link to Article
Imperiale  TFWagner  DRLin  CYLarkin  GNRogge  JDRansohoff  DF Risk of advanced proximal neoplasms in asymptomatic adults according to the distal colorectal findings. N Engl J Med 2000;343169- 174
PubMed Link to Article
Rex  DK The small polyp at flexible sigmoidoscopy: an historical perspective on why practices still vary. J Clin Gastroenterol 1999;2819- 22
PubMed Link to Article
Dave  SHui  SKroenke  KImperiale  TF Is the distal hyperplastic polyp a marker for proximal neoplasia? J Gen Intern Med 2003;18128- 137
PubMed Link to Article
Lewis  JDNg  KHung  KE  et al.  Detection of proximal adenomatous polyps with screening sigmoidoscopy: a systematic review and meta-analysis of screening colonoscopy. Arch Intern Med 2003;163413- 420
PubMed Link to Article
Egger  MSmith  GDAltman  DG Systematic Reviews in Health Care: Meta-analysis in Context. 2nd ed. London, England BMJ Books2001;
Petitti  DB Meta-analysis, Decision Analysis and Cost-effectiveness Analysis. 2nd ed. New York, NY Oxford University Press2000;
Hofstad  BVatn  MHAndersen  SN  et al.  Growth of colorectal polyps: redetection and evaluation of unresected polyps for a period of three years. Gut 1996;39449- 456
PubMed Link to Article
Lemon  SZapka  JPuleo  ELuckmann  RChasan-Taber  L Colorectal cancer screening participation: comparisons with mammography and prostate-specific antigen screening. Am J Public Health 2001;911264- 1272
PubMed Link to Article
Sutton  AJAbrams  KRJones  DRSheldon  TASong  F Methods for Meta-analysis in Medical Research.  New York, NY John Wiley & Sons2000;

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