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Ileoanal pouch cancers in ulcerative colitis and familial adenomatous polyposis: A systematic review and meta-analysis

  • Danujan Sriranganathan
    Affiliations
    Department of Medicine, Northwick Park Hospital, London North West University Healthcare NHS Trust, Harrow, HA1 3UJ, United Kingdom
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  • Danilo Vinci
    Affiliations
    Department of Surgical Science, University Tor Vergata, 00133, Rome, Italy
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  • Gianluca Pellino
    Correspondence
    Corresponding author at: Department of Advanced Medical and Surgical Sciences, Università degli Studi della Campania “Luigi Vanvitelli”, Naples, Italy/Vall d'Hebron University Hospital, Barcelona, Spain.
    Affiliations
    Department of Advanced Medical and Surgical Sciences, Universitá degli Studi della Campania "Luigi Vanvitelli", Naples, Italy

    Colorectal Surgery, Vall d'Hebron University Hospital, Barcelona, Spain
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  • Author Footnotes
    1 Guarantor of article: Jonathan P. Segal
    Jonathan P. Segal
    Footnotes
    1 Guarantor of article: Jonathan P. Segal
    Affiliations
    Department of Gastroenterology, Northern Hospital, Epping, Melbourne, Australia

    Department of Medicine, University of Melbourne, Parkville, Melbourne, Australia
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  • Author Footnotes
    1 Guarantor of article: Jonathan P. Segal

      Abstract

      Introduction

      Restorative proctocolectomy results in the formation of a pouch that adapts to a more colonic phenotype. The incidence of cancer of the pouch is thought to be low with most societal guidelines differing on their recommendations for surveillance.

      Aims

      We conducted a systematic review with meta-analysis to report the incidence of cancer in all pouch patients.

      Methods

      The Embase, Embase classic and PubMed databases were searched between June 1979– June 2021. A random effects model was performed to find the pooled incidence of pouch cancer. In addition, we also looked for risk factors for pouch cancers.

      Results

      Forty-six studies were included. In 19,964 patients with Ulcerative Colitis (UC) the pooled incidence of pouch cancer was 0.0030 (95% CI: 0.0016 -0.0055). In 3741 patients with Familial Adenomatous Polyposis (FAP) the pooled incidence of pouch cancer was 0.01 (95% CI: 0.01 – 0.02). In UC most pouch cancers were found to occur in the pouch body (0.59 (95% CI: 0.29–0.84)).

      Conclusions

      The findings suggest that the pooled incidence of pouch cancer in UC is similar to that which was previously published, and this is the first meta-analysis to report a pooled incidence for pouch cancer in FAP.

      Keywords

      1. Introduction

      Restorative proctocolectomy (RPC) refers to the operation where the diseased large bowel is removed, and the patient's own small bowel is constructed into a reservoir where defaecation can occur. The procedure is most commonly carried out in patient with ulcerative colitis (UC), Familal adenomatous polyposis (FAP), and Crohn's disease (CD). The pouch is well known to adapt to a more colonic phenotype, but the incidence of pouch cancers is thought to be low [
      • Shen B.
      • Kochhar G.S.
      • Kariv R.
      • Liu X.
      • Navaneethan U.
      • Rubin D.T.
      • et al.
      Diagnosis and classification of ileal pouch disorders: consensus guidelines from the International Ileal Pouch Consortium.
      ]. Despite this, most societal guidelines suggest ongoing surveillance of the pouch at different time intervals dependent on risk factors such as coexistence of primary sclerosing cholangitis (PSC), type C pouch mucosa, and pre-existence of dysplasia or cancer in the colectomy specimen [
      • Derikx L.A.A.P.
      • Nissen L.H.C.
      • Oldenburg B.
      • Hoentjen F.
      Controversies in pouch surveillance for patients with inflammatory bowel disease.
      ]. Type C mucosa is defined as a pattern of persistent atrophy with severe inflammation and thus is more prone to develop into cancer [
      • Sarigol S.
      • Wyllie R.
      • Gramlich T.
      • Alexander F.
      • Fazio V.
      • Kay M.
      • et al.
      Incidence of dysplasia in pelvic pouches in pediatric patients after ileal pouch-anal anastomosis for ulcerative colitis.
      ]. Pouch cancer has been reported as being rare with a systematic review in 2014 by Selvaggi et al. highlighting a pooled cumulative incidence of pouch-related adenocarcinoma of 0.35% after 20 years after RPC for UC [
      • Selvaggi F.
      • Pellino G.
      • Canonico S.
      • Sciaudone G.
      Systematic review of cuff and pouch cancer in patients with ileal pelvic pouch for ulcerative colitis.
      ]. In FAP the data is scarce with no pooled incidence data being published to date [
      • le Cosquer G.
      • Buscail E.
      • Gilletta C.
      • Deraison C.
      • Duffas J.-.P.
      • Bournet B.
      • et al.
      Incidence and risk factors of cancer in the anal transitional zone and ileal pouch following surgery for ulcerative colitis and familial adenomatous polyposis.
      ].
      Understanding the incidence of pouch cancers can aid the optimisation of surveillance strategies and help uniform guidelines to help reduce the risk of pouch cancers. Importantly, pouch cancers are associated with significant morbidity and mortality, hence early detection and optimal screening is vital to improve outcomes.
      This systematic review with meta-analysis therefore aims to update the systematic review from 2014, exploring the pooled cumulative incidence of all types of pouch cancers after RPC for UC, FAP, and CD.

      2. Methods

      We searched Embase and Embase classic and PubMed from June 1979 to June 2021 to identify cross sectional studies that reported the incidence of pouch cancers in adults. To identify published abstracts, we hand searched conference proceedings from United European Gastroenterology Week, European Crohn's and Colitis Organisation congress, British Society of Gastroenterology and Digestive Disease Week) up to June 2021.
      We searched the medical literature using the terms in Supplementary Table 1 using both as medical subject headings [MeSH] and free-text terms. No language restrictions were applied. We hand searched references from eligible studies for any further studies to be included. For studies that appeared potentially eligible but did not have the required data, we emailed the authors for clarification. The eligibility of studies was independently assessed by two authors (DS and DV). All disagreements went to a third reviewer (JPS) for a consensus.

      2.1 Inclusion and exclusion criteria

      Cross sectional and population-based studies where the majority (>90%) of the patients were 18 years of age or older were included. The studies had to have reported an incidence of pouch cancer in their cohort of patient with those patients having a diagnosis of UC, FAP, or CD. In addition, studies conducted using registries involving UC, FAP, or CD patients to calculate a incidence of pouch cancers were included. Case reports and cohort studies with less than 5 patients were excluded.

      2.2 Data analysis

      We collected data on: country, type of pouch, median/mean age of pouch, years of disease before RPC, years between RCP and cancer, presence of dysplasia in pre-colectomy sample, prior rectal cancers, presence of pouchitis, presence of PSC, tumour location, outcome of tumour treatment (alive/ died), months of follow-up post diagnosis of tumour, number of male or female patients. We assessed the quality of studies using the Joanna Briggs Institute (JBI) Prevalence Critical Appraisal Checklist for studies reporting prevalence and incidence data, with studies scoring less than 6/9 being excluded [
      • Munn Z.
      • Moola S.
      • Lisy K.
      • Riitano D.
      • Tufanaru C.
      Methodological guidance for systematic reviews of observational epidemiological studies reporting prevalence and cumulative incidence data.
      ].
      We combined the proportion of patients with pouch cancer in each study to give a pooled incidence for each study. We then performed a random effects model in order to pool the data to provide an estimate of incidence of pouch cancer. Heterogeneity was assessed using the I2 statistic. Potential risk factors were evaluated by means of odds ratio (OR) with 95% confidence intervals (CI). P < 0.05 was considered statistically significant.
      Sensitivity analysis was performed using one-study remove method to detect the impact of each study on the combined effect. Publication bias was assessed by funnel plot inspection, Egger's test, and Begg's test. All statistics were performed using R with the package “meta”.
      The systematic review followed a prior defined protocol with comprehensive search of multiple electronic databases including conference proceedings, and followed steps as recommended in the PRISMA guidelines for reporting systematic reviews [
      • Page M.J.
      • McKenzie J.E.
      • Bossuyt P.M.
      • Boutron I.
      • Hoffmann T.C.
      • Mulrow C.D.
      • et al.
      The PRISMA 2020 statement: an updated guideline for reporting systematic reviews.
      ]. The protocol was assigned a registration number of CRD42021267496 by Prospero.

      3. Results

      The search revealed 4531 studies. After abstract screening there were 53 studies remaining and after full text screening, 46 studies were analysed (Fig. 1). The 46 studies reported on 23,705 patients with an average follow up of 109 months. Due to a lack of published data for Crohn's disease analysis was not possible, thus only findings for UC and FAP have been reported. The characteristics of the studies are displayed in Table 1.
      Table 1Characteristics of studies included.
      AuthorYearCountryTotal cohortPercentage femaleNumber with UC (Pouch cancer)Number with FAP (Pouch cancer)Average follow up of cohort (months)
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      2016Belgium166Not stated109(0)57(0)114 FAP /60 UC
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      3.1 Incidence of pouch cancer in UC

      Twenty-eight studies reported on 19,964 patients with 73 cases of pouch cancer being found. This produced a pooled incidence of 0.0030 (95% CI: 0.0016 −0.0055) (Fig. 2a) with a significant heterogeneity (I2= 80%, p <0.01). Eggers' test indicated the presence of funnel plot asymmetry suggesting publication bias (P = 0.02) (Supplementary Figure 1).
      Fig. 2
      Fig. 2(a): Forest plot of studies reporting pouch cancer in patients with UC. (b): Forest plot of studies reporting pouch cancer in patients with FAP.

      3.2 Incidence of pouch cancer in FAP

      Twenty-two studies reported on 3741 patients with 68 cases of pouch cancer being found. This produced a pooled incidence of 0.01 (95% CI: 0.01 – 0.02) (Fig. 2b) with a significant heterogeneity (I2= 66%, p <0.01). Eggers’ test indicated the presence of funnel plot asymmetry suggesting publication bias (P = 0.001) (Supplementary Figure 2).

      3.3 Mixed effects regression

      With the incidence data for both UC and FAP pooled; mixed effects regression (Fig. 3) did not suggest an association between the year of publication of the study and the size of effect (14.9 95% CI: 158.3–188.2) (P = 0.86).
      Fig. 3
      Fig. 3Bubble plot of all the studies reporting pouch cancer.

      3.4 Effect of pouchitis on pouch cancer

      Three studies reported on the number of patients with UC who developed pouchitis and the incidence of cancer. This included 2236 patients with 132 having at least one of episode of pouchitis. Of the patients with pouchitis, three developed pouch cancer compared to none in those without pouchitis. Due to the rarity of the cases and large heterogeneity further analysis was not carried out.

      3.5 Effect of hand-sewn procedure vs stapled on pouch cancer

      For patients with UC, four studies reported the type of procedure used to create the ileal pouch-anal anastomosis (IPAA) and the incidence of cancer. This included 2141 patients with 147 patients undergoing stapled and 1994 undergoing hand-sewn IPAA. Two patients with stapled anastomosis went on to develop pouch cancer and four with hand-sewn anastomosis. Due to the rarity of the cases and large heterogeneity further analysis was not carried out.

      3.6 Location of cancer in the pouch

      Twenty-eight studies reported on the location of the cancer in the pouch in patients with UC. There were 53 cases in the pouch body, 17 in the anal transition zone (ATZ) and 3 in the rectal pouch. In the pouch body there is a reported pooled incidence of 0.59 (95% CI: 0.29–0.84) without significant heterogeneity (I2=0% P = 1) (Fig. 4a). Eggers’ test did not indicate the presence of funnel plot asymmetry suggesting absence of publication bias (P = 0.19) (Supplementary Figure 3). At the ATZ there is a reported pooled incidence of 0.24 (95% CI: 0.10–0.49) without significant heterogeneity (I2=0% P = 1) (Fig. 4b). Eggers’ test did not indicate the presence of funnel plot asymmetry suggesting absence of publication bias (P = 0.53) (Supplementary Figure 4). In the rectal pouch there is a reported pooled incidence of 0.00 (95% CI: 0.00 −1.00) (Fig. 4c) without significant heterogeneity (I2=0% P = 1). Eggers’ test did not indicate the presence of funnel plot asymmetry suggesting absence of publication bias (P = 0.85) (Supplementary Figure 5). An absence of sufficient data in patient with FAP meant that an analysis could not be performed. However, the extracted data is available to be viewed in Supplementary Table 4.
      Fig. 4
      Fig. 4(a): Forest plot of studies reporting pouch cancer in the pouch body in patients with UC. (b): Forest plot of studies reporting pouch cancer in the ATZ in patients with UC. (c): Forest plot of studies reporting pouch cancer in the rectal pouch in patients with UC.

      4. Discussion

      This study updates and expands on the previous meta-analysis performed by Selvaggi et al. on pouch adenocarcinomas after RPC in UC patients [
      • Selvaggi F.
      • Pellino G.
      • Canonico S.
      • Sciaudone G.
      Systematic review of cuff and pouch cancer in patients with ileal pelvic pouch for ulcerative colitis.
      ] in 2014 and reports on 12 more studies with 97 (198%) more cases of pouch cancer identified. It demonstrates that cancer of the pouch has a pooled incidence of 0.3% in UC and 1% in FAP. In terms of location of pouch cancers our study has found that in UC 59% are found in the pouch body and 24% at the ATZ and again there was insufficient data for patients with FAP.
      The incidence of pouch cancer in UC reported by this meta-analysis is congruent to the incidence of 0.35% reported by Selvaggi et al. in 2014. With this meta-analysis including a significantly larger number of patients this will provide clinicians with more confidence when counselling patients prior to RPC as well as helping clinicians who are drafting future guidelines. This meta-analysis is also significant as it is the first to suggest a pooled incidence of pouch cancer in FAP. This is useful as it can help power future studies into the area as well as helping clinicians to make recommendations of surveillance when writing future guidelines.
      Surveillance represents the main strategy to prevent and reduce the risk of pouch cancers; it is important to identify high risk patients in order to optimise surveillance protocols and create uniform guidelines with clear indications. There is a lack of consensus in the guidelines produced internationally with regards to surveillance in UC. The British Society of Gastroenterology (BSG) [
      • Lamb C.A.
      • Kennedy N.A.
      • Raine T.
      • Hendy P.A.
      • Smith P.J.
      • Limdi J.K.
      • et al.
      British Society of Gastroenterology consensus guidelines on the management of inflammatory bowel disease in adults.
      ] recommend 5 yearly or no surveillance in those with no high-risk features whereas the European Crohn's and Colitis Organisation (ECCO) [
      • Annese V.
      • Beaugerie L.
      • Egan L.
      • Biancone L.
      • Bolling C.
      • Brandts C.
      • et al.
      European Evidence-based Consensus: inflammatory Bowel Disease and Malignancies.
      ] and American Society for Gastrointestinal Endoscopy (ASGE) [
      • Shergill A.K.
      • Lightdale J.R.
      • Bruining D.H.
      • Acosta R.D.
      • Chandrasekhara V.
      • et al.
      American Society for Gastrointestinal Endoscopy Standards of Practice Committee
      The role of endoscopy in inflammatory bowel disease.
      ] make no specific recommendation on the indication to and frequency of endoscopy in these patients. However, all three organisations do agree that in patients deemed high risk, yearly surveillance is warranted. Comparing the differences between the organisations is beyond the scope of this meta-analysis but is well documented by Derikx et al. [
      • Derikx L.A.A.P.
      • Nissen L.H.C.
      • Oldenburg B.
      • Hoentjen F.
      Controversies in pouch surveillance for patients with inflammatory bowel disease.
      ]. Our results also add further weight to the current guidelines for FAP which recommend earlier and more frequent surveillance than in UC. For example, the American Society for Gastrointestinal Endoscopy suggesting a first endoscopy 1 year after the procedure with regular surveillance 1–2 yearly in all patients with FAP [
      • Yang J.
      • Gurudu S.R.
      • Koptiuch C.
      • Agrawal D.
      • Buxbaum J.L.
      • Abbas Fehmi S.M
      • et al.
      American Society for Gastrointestinal Endoscopy guideline on the role of endoscopy in familial adenomatous polyposis syndromes.
      ].
      Our findings also suggest that cancer is more commonly found in the pouch body which agrees with most of the current discussions on whether pouch cancer arises from dysplasia of the ileal mucosa itself or from residual viable rectal mucosa islets. It has been demonstrated, through clinical studies, the mucosal capability to regenerate and the possibility for the neoplasia to origin from the colonized ileal mucosa or the residual mucosa. The theory of the colonized ileal mucosa is supported by the finding of ileal pouch mucosal dysplasia and aneuploidy that have been reported; even though most of the studies have detected inflammatory changes or villous atrophy with hyperplasia, without any colonic metaplasia [
      • Bentrem D.J.
      • Wang K.L.
      • Stryker S.J.
      Adenocarcinoma in an ileal pouch occurring 14 years after restorative proctocolectomy: report of a case.
      ,
      • Rotholtz N.A.
      • Pikarsky A.J.
      • Singh J.J.
      • Wexner S.D.
      Adenocarcinoma arising from along the rectal stump after double-stapled ileorectal J-pouch in a patient with ulcerative colitis: the need to perform a distal anastomosis. Report of a case.
      ]. These findings can help endoscopists better target surveillance.
      There are several limitations to this study, many of which are inherent to meta-analyses, meaning that the results should be interpreted with caution. Due to the relative rarity of malignancy of the pouch and the limited research in the area there was a small number of patients included. Also, the studies included were all observational cohort studies with significant heterogeneity in the data. This may lead to result selection bias. The heterogeneity is accounted for in the wide range of risk factors that can contribute to the development of malignancies and the inability to separate these adequately when studying a cohort.
      This meta-analysis has shown that the incidence of pouch cancers in UC appears to have been stable over the last 7 years. It is also the first to suggest a pooled incidence rate for FAP which while is higher than for UC is lower than rates quoted in the literature. The findings should be considered when counselling patients prior to an RPC as well as when new guidelines into the surveillance of pouch cancers are developed. However, national and international co-operation is required to pool multicentre data sets which will improve granularity in the data.

      CRediT authorship contribution statement

      Danujan Sriranganathan: Data curation, Writing – original draft. Danilo Vinci: Data curation, Writing – original draft. Gianluca Pellino: Conceptualization, Writing – review & editing. Jonathan P. Segal: Conceptualization, Formal analysis, Writing – original draft.

      Conflict of interest

      J.P.S. has received speaker fees for Janssen, Abbvie and Takeda; D.S., D.V. and G.P. have no conflict of interest to disclose.

      Funding

      None to declare.

      Data Availability Statement

      The data underlying this article are available in the article and in its online supplementary material.

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