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Background

Bowel symptoms are often considered an indication to perform colonoscopy to identify or rule out colorectal cancer or precancerous polyps. Investigation of bowel symptoms for this purpose is recommended by numerous clinical guidelines. However, the evidence for this practice is unclear. The objective of this study is to systematically review the evidence about the association between bowel symptoms and colorectal cancer or polyps.
Methods

We searched the literature extensively up to December 2008, using MEDLINE and EMBASE and following references. For inclusion in the review, papers from cross sectional, case control and cohort studies had to provide a 2×2 table of symptoms by diagnosis (colorectal cancer or polyps) or sufficient data from which that table could be constructed. The search procedure, quality appraisal, and data extraction was done twice, with disagreements resolved with another reviewer. Summary ROC analysis was used to assess the diagnostic performance of symptoms to detect colorectal cancer and polyps.
Results

Colorectal cancer was associated with rectal bleeding (AUC 0.66; LR+ 1.9; LR- 0.7) and weight loss (AUC 0.67, LR+ 2.5, LR- 0.9). Neither of these symptoms was associated with the presence of polyps. There was no significant association of colorectal cancer or polyps with change in bowel habit, constipation, diarrhoea or abdominal pain. Neither the clinical setting (primary or specialist care) nor study type was associated with accuracy.

Most studies had methodological flaws. There was no consistency in the way symptoms were elicited or interpreted in the studies.
Conclusions

Current evidence suggests that the common practice of performing colonoscopies to identify cancers in people with bowel symptoms is warranted only for rectal bleeding and the general symptom of weight loss. Bodies preparing guidelines for clinicians and consumers to improve early detection of colorectal cancer need to take into account the limited value of symptoms.
Keywords:
colorectal cancer; colorectal polyps; bowel symptoms; rectal bleeding; change in bowel habit
Background

Adenocarcinoma of the colon and rectum is the third most common cancer and the third leading cause of death in the United Kingdom. In 2004, there were almost 40,000 new cases diagnosed, and about 16,000 deaths from colorectal cancer [1]. The symptoms with which colorectal cancer are purported to present most commonly include alteration in bowel habit, rectal bleeding, abdominal pain and weight loss [2,3].

Bowel symptoms occur commonly in the community and are often self limiting. There is little information available about why or when people seek medical attention for them [4,5]. Colonoscopies to exclude colorectal cancer are done frequently for a wide range of bowel symptoms, a practice suggested by guidelines [6] although it is unclear which symptoms, if any, improve the diagnostic yield of cancers or polyps. The costs, both clinical and financial, of performing colonoscopies are high. To inform policy, it is therefore important to assess which symptoms, if any, are associated with cancer and precancerous polyps.

The aim of this systematic review was to assess the evidence about the association between bowel symptoms and colorectal cancer or colorectal polyps.
Methods
Search strategy

We conducted a comprehensive search of the health literature for all studies evaluating symptoms and colorectal cancer or polyps. The search was undertaken in December 2008 to identify relevant studies. We searched MEDLINE (1966-2008) and complete EMBASE, using a list of symptoms and diagnoses as MeSH headings; the full search strategy is given in Additional File 1. The literature selection was based initially on the paper title, and if thought relevant, followed in turn by the abstract or full paper. Foreign language papers were translated into English. The literature search and selection of papers for full review, was carried out independently on two occasions 6 months apart by one reviewer.

Additional file 1. Full search strategy (medline)

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Further, the references included in all selected papers, as well as review articles, were assessed for possible inclusion in the systematic review. The citations for each paper identified for inclusion in the review were also checked using the cited reference component of the Web of Science database.
Inclusion criteria

For inclusion in the review, papers had to provide sufficient data about both the symptom and diagnosis (colorectal cancer or polyps) and provide a 2×2 table of symptoms by diagnosis, or the data from which that table could be constructed. We did not restrict included papers to certain study types, and we have extensively explored whether study characteristics had any effect on the findings. Papers (n = 8) that did not differentiate between cancers and polyps were excluded. Only full papers were included: where a relevant conference abstract was found, the literature was searched for a more detailed description of the study. If no full paper was found, the abstract was not included (this occurred with 1 abstract) [7].
Data extraction and methodological assessment

Extraction of data was performed by one reviewer (BA), with the complete set of data extracted independently on two separate occasions 6 months apart. Issues of uncertainty or discrepancy between the data extraction sets were referred to a second reviewer (LI); this occurred in 50% of papers. Agreement was subsequently obtained at consensus meetings.

For each study, data about methodology, quality and population characteristics were extracted. Items assessed included the clinical setting of the study, whether all participants had at least one symptom or some were asymptomatic (population type), whether each participant could have only one or more than one symptom reported, and study design items (patient recruitment from general or specialist practice settings, prospective or retrospective data collection, year of publication, consecutive patient recruitment, study type, reference standard used), and the ease with which data could be extracted from the paper. We also assessed the prevalence of cancer in each paper. The data categories and the assumptions required to extract the data are shown in Additional File 2.

Additional file 2. data categories and the assumptions required to extract the data

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One paper described two studies, for which we combined the data [8]. In the same paper, there were 'don't know' responses that were categorised as "present" for our analysis. This did not occur in more than 4.4% of responses.

We used colorectal cancer and polyps only as the two main outcome measures. Colorectal cancer included colon and rectal cancer, and included cancers that were confirmed by histology, as well as cancers listed as such in the papers but with no criteria given for the diagnosis. In general, papers providing information about polyps did not differentiate between polyps greater or less than 10 mm, or between different polyp histology; results are therefore for all polyps.

We have presented results for all symptoms for cancer, but for polyps and for comparisons between cancer and polyps we have included results only for those symptoms which showed a significant association for cancer.
Statistical method

The estimated sensitivity and specificity were used to estimate the diagnostic odds ratio (DOR (=[sensitivity/(1-sensitivity)]/[(1-specificity)/specificity]) which provides a single summary measure of test accuracy for each study. A high DOR indicates high test accuracy; a test that performs no better than chance in discriminating between diseased and non-diseased persons has a DOR of one. Summary ROC (SROC) methods were used to investigate the accuracy of symptoms for the diagnosis of colorectal cancer (or polyps); and to investigate whether study methodology, quality and population characteristics were associated with the diagnostic performance of symptoms. Preliminary exploratory analyses for each symptom were conducted using the SROC linear regression method of Moses and Littenberg [9]. The loge(DOR) was modeled (using unweighted least squares) as a function of the underlying test positivity rate (logit (sensitivity) + logit(1-specificity)) which is a proxy for test threshold. Study and patient characteristics were fitted as covariates. Regression diagnostics were examined to identify outliers and potentially influential studies in determining the shape and position (accuracy) of the SROC curve.

Studies were further analysed using the hierarchical SROC (HSROC) model of Rutter and Gatsonis [10,11]. This mixed model is more complex, but more rigorous that the Moses and Littenberg method because it takes separate account of the uncertainty in the estimates of sensitivity and specificity within each study, and includes random study effects for both test accuracy and positivity criterion (proxy for threshold), thereby taking account of unexplained heterogeneity between studies. The model also allows test accuracy to vary with "threshold" through the inclusion of a scale (shape) parameter fitted as a fixed effect which provides for asymmetry in the SROC. Fixed effect covariates were fitted to assess whether accuracy, positivity criterion or the shape of the SROC was associated with study or patient characteristics. Empirical Bayes estimates of model parameters were obtained using PROC NLMIXED in SAS [12]. These parameter estimates were used to obtain summary estimates and 95% confidence intervals for sensitivity and specificity (summary operating point), and likelihood ratios. The area under the SROC curve (AUC) was computed using numerical integration. Where the summary curve was symmetric, the DOR is also reported as it is constant across all thresholds.

Covariates that showed at least very weak association (p < 0.25) with diagnostic performance in the preliminary analysis were included in the model to assess whether test accuracy, the positivity criterion and/or the shape of the SROC varied with population and study design characteristics. The chosen level for statistical significance was 5% (two sided). Where summary ROC curves being compared had the same shape, the relative DOR (RDOR) was used as the summary measure of the relative diagnostic performance, otherwise the AUC was used. Only results that were robust to the removal of an influential study are reported.

Comparison of the accuracy of each symptom for the diagnosis of colorectal cancer versus polyps was restricted to studies that provided data for both outcomes. This "paired" analysis, where the diagnosis is fitted as a covariate in the HSROC model, ensures that the comparison is not confounded by study or patient characteristics.

The fitted summary ROC curves derived from the HSROC model are displayed in ROC space, and are superimposed on the study specific estimates of sensitivity and specificity that are denoted by an ellipse. The horizontal and vertical dimensions of each ellipse are proportional to the square root of the number of non-diseased and diseased respectively. A cross is used to show the summary estimate of sensitivity and specificity. For the "paired" analyses, the two points for each study are joined by a line; points are denoted by circles that do not vary in size for the sake of clarity for these plots.
Ethics approval

As this is a systematic review conducted on previously published papers and did not use patient level data, no approval was required.
Results

The literature search yielded 14,121 articles, of which 248 were selected for full review. Three non-English papers were translated but only one met the inclusion criteria. We identified 62 eligible papers that provided relevant information separately for cancers and polyps [8,13-73]. Studies were published between 1960 and 2008. Quality and study characteristics and descriptors are shown in Additional File 2.

There was a wide range of symptoms included in the papers, with many papers providing information on several symptoms: 26 separate symptoms were included, as well as 3 combinations of symptoms (for example, bleeding together with change in bowel habit). In addition, some papers provided information about descriptions of bleeding. A full list of papers, with all outcomes, and symptoms is provided in Additional File

Colon Cancer Symptoms 

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Colon Cancer Symptoms 

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Colon Cancer Symptoms 

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Colon Cancer Symptoms 

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Colon Cancer Symptoms 

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Colon Cancer Symptoms 

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Colon Cancer Symptoms 

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Colon Cancer Symptoms 

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Colon Cancer Symptoms 

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Colon Cancer Symptoms 

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Colon Cancer Symptoms 

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