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The British Journal of Radiology logoLink to The British Journal of Radiology
. 2022 Jul 21;95(1137):20220152. doi: 10.1259/bjr.20220152

Risk of developing gallbladder cancer in patients with gallbladder polyps detected on transabdominal ultrasound: a systematic review and meta-analysis

Kieran G Foley 1,✉, Zena Riddell 2, Bernadette Coles 3, S Ashley Roberts 4, Brian H Willis 5
PMCID: PMC10996949  PMID: 35819918

Abstract

Objective:

To estimate the risk of malignancy in gallbladder polyps of incremental sizes detected during transabdominal ultrasound (TAUS).

Methods:

We searched databases including MEDLINE, Embase, and Cochrane Library for eligible studies recording the polyp size from which gallbladder malignancy developed, confirmed following cholecystectomy, or by subsequent follow-up. Primary outcome was the risk of gallbladder cancer in patients with polyps. Secondary outcome was the effect of polyp size as a prognostic factor for cancer. Risk of bias was assessed using the Quality in Prognostic Factor Studies (QUIPS) tool. Bayesian meta-analysis estimated the median cancer risk according to polyp size. This study is registered with PROSPERO (CRD42020223629).

Results:

82 studies published since 1990 reported primary data for 67,837 patients. 67,774 gallbladder polyps and 889 cancers were reported. The cumulative median cancer risk of a polyp measuring 10 mm or less was 0.60% (99% credible range 0.30–1.16%). Substantial heterogeneity existed between studies (I2 = 99.95%, 95% credible interval 99.86–99.98%). Risk of bias was generally high and overall confidence in evidence was low. 13 studies (15.6%) were graded with very low certainty, 56 studies (68.3%) with low certainty, and 13 studies (15.6%) with moderate certainty. In studies considered moderate quality, TAUS monitoring detected 4.6 cancers per 10,000 patients with polyps less than 10 mm.

Conclusion:

Malignant risk in gallbladder polyps is low, particularly in polyps less than 10 mm, however the data are heterogenous and generally low quality. International guidelines, which have not previously modelled size data, should be informed by these findings.

Advances in knowledge

This large systematic review and meta-analysis has shown that the mean cumulative risk of small gallbladder polyps is low, but heterogeneity and missing data in larger polyp sizes (>10 mm) means the risk is uncertain and may be higher than estimated.

Studies considered to have better methodological quality suggest that previous estimates of risk are likely to be inflated.

Introduction

Gallbladder polyps are commonly detected in adults during transabdominal ultrasound examination (TAUS). 1 Gallbladder polyps can be separated into two categories; true polyps, or adenomas, that have malignant potential, and pseudopolyps consisting predominately of cholesterol, which have no malignant potential at all. The latter group is estimated to constitute 70% of all reported gallbladder polyps. 2

Gallbladder cancer has been shown to develop from polypoid adenomas. 3,4 More than 200,000 patients are diagnosed with gallbladder cancer each year worldwide. 5 Gallbladder cancer carries a poor prognosis (15–20% 5-year survival) because patients commonly present at an advanced stage of disease and are unsuitable for radical therapy. 6 The risk of malignant transformation of polyps to cancer is thought to be small, however accurate estimates of risk are unknown. Predicting which of the many patients with gallbladder polyps will develop gallbladder cancer is extremely difficult, but clinically important.

The assessment and monitoring of gallbladder polyps represent an ongoing clinical challenge that requires considerable resources from radiology departments around the world. Several international societies have attempted to provide evidence-based clinical guidance, based on size thresholds for intervention. Generally, it is recommended that patients with gallbladder polyps measuring 10 mm or more should undergo cholecystectomy. Recently updated European guidelines 7 recommend ultrasound monitoring for up to 2 years in patients with polyps measuring 6 mm or more, provided polyp size is stable, or for polyps 5 mm or less if risk factors are present. In contrast, the Canadian Association of Radiologists recently endorsed the American College of Radiology recommendations that surveillance of polyps measuring 7 mm or more should be performed for up to 2 years, with polyps less than 7 mm not requiring follow-up. 8 The available evidence is largely considered to be low quality, 1,2,9–11 and international guidance has never modelled polyp size for malignant risk to justify their recommendations for appropriate intervention. Additional limitations include strong selection, detection, and reporting bias which significantly hinders confidence in any current estimated malignant risk.

Therefore, to address this gap, a systematic review and meta-analysis was conducted to establish the overall risk of gallbladder cancer in patients with polyps detected by TAUS. We examined TAUS measured polyp size as a prognostic factor for gallbladder cancer and explored other potentially important clinical co-variates for their associated malignant risk.

Methods and materials

This study was prospectively registered with PROSPERO (CRD42020223629) and results were reported following the Preferred Reporting Items for Systematic Reviews and Meta-analysis (PRISMA) guidelines. 12

Search strategy

A comprehensive search strategy using Medical Subject Headings (MeSH) and free-text terms was designed for this systematic review using MEDLINE. This strategy was adapted to run in the following electronic databases: MEDLINE, Embase, Cochrane Library, Cumulative Index of Nursing and Allied Health Literature (CINAHL), Scopus, Web of Science, and ClinicalTrials.gov. (Supplementary Material 1) The initial search was performed on October 28, 2020, and updated on December 4, 2020. The search was limited to English language.

Study selection

The systematic review included randomised control trials, observational cohort, cross-sectional and case–control studies published since 1990. We included studies that reported consecutive or random primary data in adult participants (18 years or older), diagnosed with a gallbladder polyp on TAUS, that recorded the size of polyp from which a gallbladder malignancy occurred, confirmed either following cholecystectomy, or by monitoring the polyp to determine its natural history. A monitoring period of at least 12 months was required. A polyp is often termed a mass once it measures 30 mm, however, to maximise the capture of continuous data, sizes of polypoid lesions more than 30 mm were also recorded. Studies were excluded that did not contain any primary data or did not provide polyp or cancer measurements. Attempt was made to discover translations of any non-English language article that was inadvertently retrieved. Reference lists of all eligible studies were checked and underwent citation tracking for additional eligible studies. Search of the grey literature was not performed.

Outcomes

The pre-specified primary outcome was the risk of gallbladder cancer in adult patients with polyps detected by TAUS. The secondary outcome was the effect of polyp size as a prognostic factor for gallbladder cancer. Additional secondary outcomes were the malignant risk of associated clinical co-variates: age at diagnosis, gender, presence of gallstones, presence of symptoms, and the presence of single or multiple polyps.

Data extraction

Two investigators (KGF/ZR) independently screened all titles and abstracts, assessed full texts for eligibility, and extracted data based on the CHARMS 13 and CHARMS-PF 14 checklists. Disagreements were resolved after review by a third investigator (SAR). Data extracted (Supplementary Material 1) included study identifiers, study design, setting and population characteristics, sample size, polyp and cancer size, and follow-up. Where an included study reported missing data, the corresponding author was contacted inviting them to share the complete data set.

Quality assessment

Risk of bias was assessed using the Quality in Prognostic Factor Studies (QUIPS) tool for each study. 15 The strength of the overall weight of evidence for both primary and secondary outcomes was judged using the Grading of Recommendations Assessment, Development and Evaluation (GRADE) working group methodology. 16 (Supplementary Material 1)

Data analysis

A Bayesian meta-analysis model which incorporated the effects of polyp size and other covariates on the risk of cancer was developed. This was a random intercept and random gradient model to allow the effects of polyp size on the risk of cancer to vary across studies. The model was expanded to account for extensive missing data amongst the response and the predictor variables. The data were modelled by assuming separate multinomial distributions for the number of cancers and polyps at different sizes and imputing new data for each iteration of the Bayesian model. As a result, all eligible studies could be included in the analysis. The model was supplemented with individual patient data, where available. The Bayesian meta-analysis model 17,18 was developed in JAGS 19 interfacing with R 20 via the rjags package. 21 (Supplementary Material 1) Between-study heterogeneity was assessed by inspection of prediction plots, and the I2 statistic. 22,23 To assess the effects of the GRADE rating on the Bayesian model, sensitivity analyses were conducted where studies rated with very low certainty were first excluded, followed by the exclusion of low and very low certainty studies.

Results

The initial search identified 3067 studies, of which 1615 were duplicates. Four additional studies were identified through other sources. The titles and abstracts of 1456 studies were screened and after screening, 1322 records were excluded for being irrelevant to this systematic review, leaving 134 full-text articles for review. Both reviewers identified 122 of the 134 full-text articles (91.0%) and the remaining 12 were included after agreement by the third reviewer. Of the 134 full-text articles, 52 were excluded (agreed by both reviewers) leaving 82 articles 24–105 published since 1990 for inclusion (Figure 1). Important characteristics of the 82 included studies are detailed in Table 1.

Figure 1.

Figure 1.

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Study selection process.

Table 1.

Studies reporting transabdominal ultrasound measurements of gallbladder polyps and malignancies that met the inclusion criteria

Author Year Country Design Sites Start date End date Patients Median age (months) Female Polyps Cancers Malignancy rate Cholecystectomy Monitoring Median follow-up (months)
Abdullah et al 24 2019 UK Retrospective 1 2011 2013 244 NR * 160 (65.6%) 201 2 1.0% 43 (21.4%) 137 (68.2%) 36
Ahmed et al 25 2013 UK Retrospective 1 2005 2010 39 51.4 29 (22.1%) 39 0 0.0% 39 (100.0%) 0 (0.0%) NR
Akyurek et al 26 2005 Turkey Retrospective 1 2000 2004 56 48 16 (28.6%) 56 0 0.0% 56 (100.0%) 0 (0.0%) NR
Al Manasra et al 27 2018 Jordan Retrospective 1 2002 2016 46 54 31 (67.4%) 46 5 7.7% 46 (100.0%) 0 (0.0%) NR
Aldouri et al 28 2009 UK Retrospective 1 1998 2006 2429 58 NR 2429 28 10.9% 2429 (100.0%) 0 (0.0%) NR
Aliyazicioglu et al 29 2017 Turkey Retrospective 1 2004 2015 185 44.6 94 (50.8%) 185 2 1.1% 185 (100.0%) 0 (0.0%) NR
Ansari et al 30 2007 Bangladesh Prospective 1 2002 2004 57 NR NR 57 1 1.8% 37 (64.9%) 26 (45.6%) 18
Azuma et al 31 2001 Japan Retrospective 1 1989 1998 89 NR NR 89 24 27.0% 89 (100.0%) 0 (0.0%) NR
Cairns et al 32 2012 UK Retrospective 1 2000 2011 986 57.1 541 (54.9%) 986 1 0.1% 134 (13.6%) 467 (47.4%) 39.3
Cha et al 33 2011 South Korea Retrospective 1 2003 2009 210 NR 101 (48.1%) 210 65 31.0% 210 (100.0%) 0 (0.0%) NR
Channa et al 34 2009 Pakistan Retrospective 1 1999 2008 28 47.5 3 (10.7%) 59 3 1.2% 28 (47.5%) 0 (0.0%) NR
Chattopadhyay et al 35 2005 UK Retrospective 1 1993 2002 23 56.8 16 (69.6%) 23 3 13.0% 23 (100.0%) 0 (0.0%) NR
Cheon et al 36 2009 South Korea Retrospective 1 1996 2006 94 50 NR 94 4 4.3% 94 (100.0%) 0 (0.0%) NR
Chijiiwa et al 37 1994 Japan Retrospective 1 1982 1990 44 NR 24 (54.5%) 44 12 27.3% 44 (100.0%) 0 (0.0%) NR
Choi et al 38 2008 South Korea Retrospective 1 2006 2007 59 NR 16 (27.1%) 262 3 5.1% 59 (22.5%) 0 (0.0%) NR
Chou et al 39 2017 Taiwan Retrospective 1 2004 2013 1204 51.8 527 (43.8%) 1204 39 3.2% 194 (16.1%) 1010 (83.9%) 72
Colecchia et al 40 2009 Italy Prospective 1 1999 2001 56 48.3 22 (39.3%) 56 0 0.0% 0 (0.0%) 53 (94.6%) 60
Collett et al 41 1998 New Zealand Prospective 1 1989 1994 38 56 NR 38 0 0.0% 0 (0.0%) 22 (57.9%) 60
Corwin et al 42 2011 USA Retrospective 1 1999 2001 346 51.6 NR 346 0 0.0% 42 (12.1%) 346 (100.0%) 96
Csendes et al 43 2001 Chile Prospective 1 1987 1996 111 47 60 (54.1%) 111 0 0.0% 27 (24.3%) 98 (88.3%) 71
Dacka et al 44 2004 Poland Retrospective 1 1998 2002 25 NR 14 (56.0%) 25 0 0.0% 25 (100.0%) 0 (0.0%) NR
Damore et al 45 2001 USA Retrospective 1 1988 1995 41 47.4 18 (43.9%) 41 0 0.0% 41 (100.0%) 0 (0.0%) NR
Donald et al 46 2013 USA Retrospective 1 2002 2011 27 NR 5 (18.5%) 27 3 11.1% 18 (66.7%) 0 (0.0%) NR
Drews et al 47 2005 Poland Retrospective 1 1993 2003 39 NR 17 (43.6%) 39 1 2.6% 39 (100.0%) 0 (0.0%) NR
Escalona et al 48 2006 Chile Retrospective 1 1991 2004 123 NR 85 (69.1%) 123 1 0.8% 123 (100.0%) 0 (0.0%) NR
French et al 49 2013 Canada Retrospective 1 2000 2010 262 49.7 184 (70.2%) 50 0 1.1% 262 (100.0%) 14 (5.3%) NR
Fujiwara et al 50 2020 Japan Retrospective 1 2003 2019 227 NR 99 (43.6%) 227 23 10.1% 227 (100.0%) 227 (100.0%) 60
Guo et al 51 2015 China Retrospective 1 1999 2012 160 NR 90 (56.3%) 160 14 8.8% 160 (100.0%) 0 (0.0%) NR
Heitz et al 52 2019 Germany Prospective Multi 2002 2013 50 57.8 NR 153 6 0.0% 0 (0.0%) 16 (32.0%) 132
Huang et al 53 2001 Taiwan Retrospective 1 1990 1998 153 NR 76 (49.7%) 62 9 3.9% 153 (100.0%) 0 (0.0%) NR
Isozaki et al 54 1995 Japan Retrospective 1 1978 1992 62 NR 31 (50.0%) 144 29 14.5% 62 (43.1%) 0 (0.0%) NR
Ito et al 55 2009 USA Retrospective 1 1996 2007 417 NR 229 (54.9%) 417 1 0.2% 80 (19.2%) 143 (34.3%) 17
Jang et al 56 2009 South Korea Prospective 1 2006 2007 144 57.6 72 (50.0%) 126 8 20.1% 144 (100.0%) 0 (0.0%) NR
Jeong et al 57 2020 South Korea Retrospective 1 2006 2017 535 NR 300 (56.1%) 535 84 15.7% 535 (100.0%) 0 (0.0%) NR
Kamali Polat et al 58 2010 Turkey Retrospective 1 Missing Missing 34 47.2 14 (41.2%) 34 1 2.9% 31 (91.2%) 0 (0.0%) NR
Khan et al 59 2012 Saudi Arabia Retrospective 1 2008 2012 26 40 19 (73.1%) 26 1 3.8% 26 (100.0%) 0 (0.0%) NR
Kim et al 60 2016 South Korea Retrospective 1 2007 2011 53 NR 27 (50.9%) 53 8 15.1% 35 (66.0%) 18 (34.0%) 46.4
Konstantinidis et al 61 2012 USA Retrospective 1 2000 2010 213 52 147 (69.0%) 213 6 2.8% 213 (100.0%) 20 (9.4%) 15.5
Koundouris et al 62 2001 Greece Retrospective 1 1994 2000 35 52 21 (60.0%) 35 7 20.0% 35 (100.0%) 0 (0.0%) NR
Kratzer et al 63 2008 Germany Prospective 1 1996 1996 31 NR 8 (25.8%) 31 0 0.0% 0 (0.0%) 22 (71.0%) 84
Kubota et al 64 1995 Japan Retrospective 1 1978 1994 72 NR 32 (44.4%) 72 16 22.2% 72 (100.0%) 12 (16.7%) 12
Kwon et al 65 2009 South Korea Retrospective 1 1992 2005 291 NR 151 (51.9%) 291 35 12.0% 291 (100.0%) 0 (0.0%) NR
Lee et al 66 2016 South Korea Retrospective 1 2002 2016 126 NR 66 (52.4%) 516 24 6.3% 126 (24.4%) 0 (0.0%) NR
Lee et al 67 2019 South Korea Retrospective 1 2005 2014 516 NR 219 (42.4%) 109 1 4.7% 516 (100.0%) 109 (21.1%) 60
Liu 68 2018 China Retrospective 1 2013 2017 109 NR 60 (55.0%) 109 23 21.1% 109 (100.0%) 0 (0.0%) NR
Maciejewski et al 69 2014 Poland Retrospective 1 2010 2013 64 52.9 NR 64 1 1.6% 64 (100.0%) 0 (0.0%) NR
Mainprize et al 70 2000 UK Retrospective 1 1993 1997 38 NR 19 (50.0%) 18 2 11.1% 34 (89.5%) 0 (0.0%) NR
Matlok et al 71 2013 Poland Retrospective 1 1997 2012 152 NR 94 (61.8%) 152 1 0.7% 152 (100.0%) 8 (5.3%) NR
Matos et al 72 2010 Portugal Retrospective 1 2003 2007 93 NR 62 (66.7%) 93 2 2.2% 86 (92.5%) 0 (0.0%) NR
Metman et al 73 2020 Netherlands Retrospective 2 2010 2010 108 56 63 (58.3%) 108 0 0.0% 108 (100.0%) 35 (32.4%) NR
Moriguchi et al 74 1996 Japan Prospective 1 1988 1988 109 54 58 (53.2%) 28 1 0.9% 0 (0.0%) 109 (100.0%) 37.2
Okamoto et al 75 1999 Japan Retrospective 1 1986 1993 1,0926 NR NR 1,0926 19 0.2% 33 (0.3%) 0 (0.0%) NR
Onda et al 76 2020 Japan Retrospective 1 2009 2014 139 NR 55 (39.6%) 139 16 11.5% 139 (100.0%) 80 (57.6%) NR
Ostapenko et al 77 2020 USA Retrospective 1 2014 2019 98 NR NR 98 0 0.0% 98 (100.0%) 0 (0.0%) NR
Park et al 78 2008 South Korea Retrospective 1 1988 2006 689 NR 542 (78.7%) 689 25 3.6% 180 (26.1%) 689 (100.0%) 60
Park et al 79 2009 South Korea Retrospective 1 1995 2005 1558 NR 723 (46.4%) 1558 34 3.6% 0 (0.0%) 1558 (100.0%) 37.2
Park et al 80 2015 South Korea Retrospective 1 1997 2012 836 47 387 (46.3%) 836 56 6.7% 836 (100.0%) 184 (22.0%) NR
Patel et al 81 2019 UK Retrospective 1 2008 2013 558 52 297 (53.2%) 558 3 0.5% 89 (15.9%) 168 (30.1%) 23.5
Pedersen et al 82 2012 Denmark Retrospective 1 2008 2009 203 54 114 (56.2%) 203 0 0.0% 13 (6.4%) 31 (15.3%) 24
Pickering et al 83 2020 Ireland Retrospective 4 2015 2018 134 53 78 (58.2%) 134 6 4.5% 134 (100.0%) 0 (0.0%) NR
Rafaelsen et al 84 2020 Denmark Prospective 1 2007 2009 154 62 100 (64.9%) 154 0 0.0% 0 (0.0%) 154 (100.0%) 120
Sahiner et al 85 2018 Turkey Retrospective 1 2008 2013 159 NR NR 159 8 5.0% 96 (60.4%) 0 (0.0%) NR
Sarici et al 86 2017 Turkey Retrospective 1 2005 2015 109 45 69 (63.3%) 109 15 2.2% 109 (100.0%) 60 (55.0%) 22.2
Sarkut et al 87 2013 Turkey Retrospective 1 1996 2012 138 55 91 (65.9%) 138 21 15.2% 138 (100.0%) 0 (0.0%) NR
Shah 88 2010 Nepal Retrospective 1 2004 2009 32 40 23 (74.2%) 32 2 6.3% 32 (100.0%) 0 (0.0%) NR
Shin et al 89 2009 South Korea Retrospective 1 1994 2007 145 48 60 (41.4%) 145 8 5.5% 145 (100.0%) 91 (62.8%) NR
Shinkai et al 90 1998 Japan Retrospective 1 1990 1995 60 NR 25 (41.7%) 60 1 13.8% 19 (31.7%) 0 (0.0%) NR
Spaziani et al 91 2019 Italy Retrospective 1 2005 2018 38 53 23 (60.5%) 38 10 26.3% 38 (100.0%) 0 (0.0%) NR
Sugiyama et al 92 2000 Japan Retrospective 1 1988 1997 194 52 105 (54.1%) 194 11 5.7% 58 (29.9%) 125 (64.4%) 31.2
Sun et al 93 2004 China Retrospective 1 1994 2002 194 45.7 101 (52.1%) 194 11 1.7% 194 (100.0%) 0 (0.0%) NR
Sun et al 94 2019 China Retrospective 1 2003 2016 686 NR 383 (55.8%) 686 10 1.5% 686 (100.0%) 686 (100.0%) 24
Sung et al 95 2014 South Korea Retrospective 1 2009 2011 228 51.6 133 (58.3%) 253 18 5.7% 253 (100.0%) 0 (0.0%) NR
Szpakowski et al 96 2020 USA Retrospective Multi 1995 2014 3,5856 50 1,8645 (52.0%) 3,5856 19 0.05% 5731 (16.0%) 3,5856 (100.0%) NR
Terzi et al 97 2000 Turkey Retrospective 1 1988 1998 100 NR 74 (74.0%) 100 26 26.0% 100 (100.0%) 0 (0.0%) NR
Terzioglu et al 98 2017 Turkey Retrospective 1 2010 2016 278 NR 187 (67.3%) 278 8 7.1% 278 (100.0%) 0 (0.0%) NR
Ungarreevittaya et al 99 2018 Thailand Retrospective 1 2017 2017 85 NR 47 (55.3%) 85 5 2.9% 85 (100.0%) 0 (0.0%) NR
Velidedeoglu et al 100 2017 Turkey Retrospective 1 2000 2012 82 48.1 47 (57.3%) 82 0 0.0% 82 (100.0%) 0 (0.0%) NR
Wu et al 101 2019 China Retrospective 1 2011 2017 1561 49.5 925 (59.3%) 1561 3 5.9% 1561 (100.0%) 0 (0.0%) NR
Xu et al 102 2017 China Retrospective 1 2008 2015 1468 NR 743 (50.6%) 1468 24 0.2% 1446 (98.5%) 0 (0.0%) NR
Yang et al 103 1992 China Retrospective 1 1982 1990 172 44.3 79 (45.9%) 172 13 7.6% 172 (100.0%) 0 (0.0%) NR
Yeh 104 2001 Taiwan Retrospective 1 1991 1999 123 NR 69 (56.1%) 123 7 1.6% 123 (100.0%) 0 (0.0%) NR
Zielinski et al 105 2009 USA Retrospective 1 1996 2007 130 NR 85 (65.4%) 130 10 7.7% 130 (100.0%) 25 (19.2%) 32
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* NR not reported. Total percentages of patients treated with cholecystectomy and monitoring may not add up to 100% (total can include patients followed-up before or after cholecystectomy and patients lost to follow-up).

The 52 excluded articles were either review articles 106–116 or systematic reviews, 2,9,10,117–120 contained no TAUS data, 121–127 were editorials, commentaries or reports, 128–134 contained insufficient clinical data, 3,135–138 contained patient cohorts previously reported, 139–142 were not available in English, 143–146 had study design not relevant for this review, 147–149 included a patient cohort not relevant to this review, 150,151 or were abstracts only. 152,153

Overall, 67,837 patients were included for evidence synthesis. In total, 67,774 gallbladder polyps and 889 gallbladder cancers were reported. The median age ranged between 40 and 62, and 57,670 were male (73.7%). All patients had gallbladder polyps detected by TAUS. In total, 20,543 were evaluated following cholecystectomy. More than half of all polyps (n = 41,041, 53.1%) were monitored with TAUS to determine their natural history. The two largest studies 75,96 provided 46,782 patients, but only 38 cancers.

There were 82 studies which provided data on the number of gallbladder polyps and cancers. 24–105 Sixty studies provided data on at least one polyp size and the associated number of gallbladder cancers that developed in polyp sizes up to 15 mm. 24–26,29–33,35–37,39–48,50,51,55,57–65,68–73,75–78,80–85,87–89,91,92,94,96,97,100,103,105 Size measurements could be extracted in 59,225 polyps and 425 malignant polyps, respectively, from these studies. In one study, the authors provided individual patient data on 558 patients. 81

16 studies (19.5%) reported cohorts with zero cancer events within the first year of follow-up. 25,26,36,40–45,49,63,73,77,82,84,100 44 studies reported non-zero cancer events in one or more polyp sizes. 24,29–33,36,37,39,50,61,64,65,68,76,78,80,81,85,88,91,92,96,97,103,105 10 studies reported on the number of cancers less than 20 mm, but not the number of polyps. 36,37,39,46,47,54,75,78,88,94

Substantial heterogeneity was measured between studies (I2 = 99.95%, 95% credible interval 99.86–99.98%). The distribution of included studies at different size thresholds is shown in Figure 2 and demonstrates the heterogeneity across studies, although most studies were concentrated in a region with a probability of cancer of less than 0.03. Data reported at subsequent time points were limited, so malignant risk over time could not be determined.

Figure 2.

Figure 2.

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Distribution of cancer risk according to gallbladder polyp size measured by transabdominal ultrasound across all included studies. Each dot represents the cancer risk at a particular polyp size for a single study. Studies which reported cancer risk at multiple polyp sizes are depicted by the line connecting the dots associated with the study. The majority of studies showed the risk of cancer to be less than 0.1 for polyp sizes up to 15 mm.

A Bayesian meta-analysis model was developed to accommodate substantial missing data across the studies. As a result, it was possible to include all 82 studies in the analysis. The model demonstrated an increased risk of cancer as polyp size increased (Figure 3a). For example, a mean polyp size of 13.9 mm had a mean risk of 1 in 100. However, there was considerable uncertainty with this estimate due to study heterogeneity and this uncertainty increased with threshold size, illustrated by the widening credible ranges, which may be explained by increased missing data at higher polyp sizes. Figure 3b shows the 95% prediction region for the predicted risk from the model. This demonstrates the effects of between-study heterogeneity on the uncertainty of the risk estimates. The prediction region is wide and increases with polyp size to around 60% suggesting substantial uncertainty in the model estimates. The addition of associated co-variates (age, gender, presence of gallstones, symptoms, and single or multiple polyps) to the model did not substantially change the Deviance Information Criterion (DIC) of the Bayesian model and therefore were excluded (Supplementary Material 1).

Figure 3.

Figure 3.

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(a) Meta-analysis summary model showing cumulative risk of gallbladder cancer as a function of polyp size and associated 95% credible interval limits (dashed lines). (b) 95% prediction regions for the estimated cumulative risk. The prediction region covers nearly all the probability space for high thresholds suggesting that the heterogeneity and missing data introduces substantial uncertainty to the model. The summary mean curve and 95% credible region are included but are close to the x-axis. The upper boundary (dashed) is readily apparent, and the lower boundary of the 95% credible region is the dashed line closest to the x-axis.

The median cancer risk of polyps measuring 5 mm and 10 mm across all studies was 0.14% (99% credible range 0.08–0.26%) and 0.60% (0.30–1.16%), respectively. Thus, the number of patients with polyps measuring 5 mm and 10 mm or less needed to detect one cancer is 714.3 and 166.7, respectively, equating to 13.2 and 64.4 cancers per 10,000 patients. The point estimates and cumulative cancer risk with 99% credible intervals for incremental polyp size is provided in Table 2. A probability matrix, showing incremental sizes of polyps with corresponding cancer risk, is included in Supplementary Material 1.

Table 2.

Point estimate and cumulative cancer risk for incremental polyp size with 99% credible intervals

Polyp size Median risk Polyp size Median risk
5 mm 0.14% (0.08–0.26%%) 23 mm 1.64% (0.79–3.25%)
6 mm 0.22% (0.12–0.42%%) 24 mm 1.70% (0.81–3.37%)
7 mm 0.31% (0.16–0.59%) 25 mm 1.76% (0.84–3.49%)
8 mm 0.41% (0.21–0.78%) 26 mm 1.82% (0.87–3.6%)
9 mm 0.51% (0.26–0.97%) 27 mm 1.87% (0.89–3.71%)
10 mm 0.60% (0.30–1.16%) 28 mm 1.92% (0.91–3.81%)
11 mm 0.70% (0.35–1.36%) 29 mm 1.97% (0.94–3.91%)
12 mm 0.80% (0.39–1.54%) 30 mm 2.02% (0.96–4.01%)
13 mm 0.89% (0.44–1.73%) 31 mm 2.07% (0.98–4.11%)
14 mm 0.98% (0.48–1.91%) 32 mm 2.11% (1.00–4.20%)
15 mm 1.06% (0.52–2.08%) 33 mm 2.16% (1.02–4.29%)
16 mm 1.14% (0.56–2.25%) 34 mm 2.20% (1.04–4.38%)
17 mm 1.22% (0.59–2.41%) 35 mm 2.24% (1.06–4.46%)
18 mm 1.30% (0.63–2.56%) 36 mm 2.28% (1.08–4.54%)
19 mm 1.37% (0.66–2.71%) 37 mm 2.32% (1.09–4.62%)
20 mm 1.44% (0.70–2.85%) 38 mm 2.36% (1.11–4.69%)
21 mm 1.51% (0.73–2.99%) 39 mm 2.39% (1.13–4.77%)
22 mm 1.58% (0.76–3.12%) 40 mm 2.43% (1.14–4.84%)
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Risk of bias assessment

The majority of studies (n = 68, 82.9%) were assessed as having high risk of bias due to their observational nature, and the remaining 14 (17.1%) as moderate risk of bias (Supplementary Material 1). According to the GRADE working group methodology, 16 13 studies (15.6%) were graded with very low certainty, 56 studies (68.3%) with low certainty, and 13 studies (15.6%) with moderate certainty (Supplementary Material 1). The overall confidence in the result of the quantitative synthesis was summarised as low.

Sensitivity analysis

The effect of methodological quality on the median cancer risk was tested in sensitivity analysis (Figure 4). Compared with the overall median curve, excluding studies with a very low certainty rating had little effect on the estimated risk. However, confining the analyses to those studies with moderate certainty or higher (13 studies) substantially lowered the median risk curve. This is due to the two largest studies, which reported only 38 cancers in 46,782 patients (0.08%), having substantially lower cancer rates than the other studies in the meta-analysis.

Figure 4.

Figure 4.

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Sensitivity analysis of cumulative risk of cancer with credible intervals related to study quality. Studies rated low certainty and above (69 studies; 66,985 patients, 870 cancers) are red. Studies rated moderate certainty and above (13 studies, 51,442 patients, 100 cancers) are blue.

In studies considered moderate quality, the median cancer risk of polyps measuring 5 mm and 10 mm or less reduced considerably to 0.03 and 0.04%, respectively. This increased the number of patients needed to detect one cancer to 2754.8 and 2167.8, equating to 3.6 and 4.6 cancers per 10,000 patients with polyps measuring 5 mm and 10 mm or less, respectively.

Discussion

This systematic review and meta-analysis of more than 67,000 patients is the first comprehensive meta-analysis to model the risk of malignancy in gallbladder polyps. The study has shown that the estimated risk of malignancy in patients with gallbladder polyps is lower than previously reported and is extremely low in polyps measuring less than 10 mm.

Presently, studies are mostly low quality which affects the estimates of malignant risk presented in this meta-analysis, however the risk of cancer reported in the two largest and higher quality studies 75,96 was far lower than the remainder of small, low-quality studies, which were likely to report inflated risk. The findings of this meta-analysis suggest that the risk of malignancy in gallbladder polyps is very low, suggesting that the monitoring of gallbladder polyps, particularly small polyps, may not be clinically or cost-effective in some healthcare systems. However, given the uncertainty introduced by the low quality studies, the clinical and cost effectiveness of monitoring small polyps requires further investigation.

Previous work has attempted to estimate the risk of malignancy in ultrasound detected gallbladder polyps. A large recent study hypothesised that the true risk of gallbladder polyps may not be as great as previously reported. A retrospective study reported outcomes of gallbladder polyps over a 20-year period in a population of more than 600,000. 96 The unadjusted gallbladder cancer rate per 100,000 person-years was 11.3 (95% confidence intervals 6.2–16.3) and increased with greater polyp size, from 1.3 (95% confidence intervals 0.7–6.5) in polyps less than 6 mm to 128.2 (95% confidence intervals 9.4–217.0) in polyps 10 mm or greater. Additionally, gallbladder cancer rates in this cohort study were similar in patients with and without polyps on initial TAUS (0.053% vs  0.054%, respectively). These data were collected retrospectively, and the proportion of pseudopolyps was not reported. The study demonstrated the apparent benign natural history and slow growth of most polyps, but firm estimates of median cancer risk cannot be extrapolated from this study due to its limitations.

Further, we have confirmed that increasing polyp size is an important prognostic factor for the development of malignancy, but an optimal size threshold for intervention remains uncertain. Gallbladder polyp size is commonly reported at TAUS because the reliability and reproducibility of size measurements is excellent. 154 The decision to intervene in patients with gallbladder polyps is contentious, but important, as many patients undergo cholecystectomy every year for gallbladder polyps. An arbitrary threshold of 10 mm is commonly cited for intervention in the literature, 39,48,65,67,79,80,86,89,102 though larger size thresholds have been reported to be more accurate at differentiating benign from malignant polyps. 33,60,68,76,95,104 Compliance with existing guidelines may have contributed to the increased detection of cancer above 10 mm in this meta-analysis, as findings were predominately derived from retrospective data, although the results demonstrated a clear continuous association with incremental polyp size without any significant step-change in risk at a particular threshold. Large-scale, prospective, multicentre registries are required to increase statistical power and provide better quality data to improve treatment and monitoring decisions in these patients. Randomised data would improve confidence in specific size thresholds.

There is also conflicting data regarding the cost-effectiveness of monitoring gallbladder polyps. Such analysis is dependent on accurate estimates of median cancer risk to provide meaningful analysis, which this meta-analysis can facilitate. Patel et al have suggested that compliance with polyp monitoring guidelines may be cost-effective. 81 The authors suggested that following the European joint society guidelines 1 would result in an estimated annual saving of £209,163 per 1000 gallbladder polyps surveyed in the National Health Service (NHS) and result in an additional 12.5% of patients requiring cholecystectomy. However, compliance with guidelines was found to be poor. 81 Indeed, poor compliance from radiology departments is likely to represent a multifactorial problem influenced by cost, patient factors, and perceived lack of value. Given our meta-analysis demonstrates a very low risk of cancer, we suggest a health economic analysis should be conducted to evaluate the clinical value of monitoring smaller gallbladder polyps.

Strengths of our study include strict adherence to methodological and reporting recommendations, robust data extraction and quality assessment. A large volume of data from many studies and patients have been synthesised. We chose to construct the meta-analysis model in a Bayesian framework to provide greater flexibility than might be possible in a frequentist framework. As a result, we were able to develop a model that included all the studies and captured the simultaneous uncertainty that missing data, between-study heterogeneity and zero event studies bring to meta-analysis. Despite these uncertainties, the model demonstrated a clear increase in cancer risk with polyp size.

However, this study also has limitations. The analysis provides an estimate for the overall cumulative risk of cancer for different polyp sizes and the uncertainty associated with this risk. However, a clinical question not answered here is that of the conditional risk of cancer for a polyp of size greater than 10 mm, for example. This would require a far more complex model and is beyond the scope of this analysis. However, for the same reasons given in the above analysis, it is likely that any estimates of the conditional risk would also be shrouded with considerable uncertainty. As such, it is worthy of further research. We included historical data using older ultrasound technology because this review was designed to assess risk rather than technology evaluation and we wanted to capture as much follow-up data as possible. Whilst measurement error is likely to be present in older cohorts, we suggest a greater number of small polyps with less risk are likely to be detected incidentally using newer ultrasound technology, and thus contribute to a further reduction in overall malignant risk. The methodological quality of the included studies was generally considered low. Suboptimal reporting of duration and frequency of follow-up in many studies prevented meaningful modelling of cancer risk in the subsequent years after detection, which would have better informed guideline recommendations for duration of follow-up. Often, patient and polyp characteristics, including proportions of true vs pseudopolyps, were inadequately reported, meaning sensitivity analyses could not be performed to explore variations on our estimated median cancer risk statistics. We had planned to include high-risk patients with primary sclerosing cholangitis (PSC) as a co-variate, however there were insufficient data to allow this. Only eight patients from two included studies were reported. 81,105 Many studies have investigated the risk of malignancy in PSC cohorts, but these can inflate the estimates in general populations and hence were excluded. Attempts were made to gather individual patient data. We received individual data from 558 patients, but the overall response rate was poor, so personalised prediction of which patients eventually developed gallbladder cancer could not be attempted. Potentially important clinical co-variates (including patient age, ethnicity, and sessile morphology) were also sporadically reported in many included studies, but addition of available co-variates in the model did not identify any factors of prognostic significance. Furthermore, any predictions are contingent on the accuracy of the model and whilst the parameter estimates were in the right direction, new trial data may refine or even challenge these. Finally, we found significant heterogeneity between studies which affected our overall confidence in the results of the meta-analysis. Publication bias could not be assessed due to the presence of intra- and inter-study heterogeneity.

Conclusion

This review is the first comprehensive meta-analysis investigating the risk of malignancy in gallbladder polyps. Here, based on the data from 67,837 patients across 82 studies, a de novo Bayesian model was developed to establish the best available estimates concerning the development of cancer risk with polyp size. Malignant risk was extremely low, particularly in polyps measuring less than 10 mm. For polyps greater than 10 mm, estimates of the actual risk were hampered by recommended intervention in this group. However, a step increase of risk in polyps measuring larger than 10 mm is neither likely, nor supported, by these data. This suggests research efforts should be directed at improved stratification of this group and potentially increasing the threshold for intervention. Other clinical risk factors usually associated with gallbladder cancer were found to have limited effect on prediction after controlling for polyp size. Substantial heterogeneity was found between studies and the quality of evidence was generally considered low. Furthermore, this review was not able to establish how the risk of gallbladder cancer evolves over time, identifying an important gap in the evidence-base and where future research should be targeted.

Supplementary Material

bjr.20220152.suppl-01
bjr.20220152.suppl-01.docx (263.2KB, docx)

Footnotes

Acknowledgements: The authors wish to acknowledge Mrs Anne Cleves for her effort obtaining the full articles for review.

Funding: No direct funding was received. KGF receives research funding from the Moondance Foundation at Velindre Cancer Centre and Health and Care Research Wales (HCRW). ZCR is supported by the Wales Cancer Research Centre and Advancing Radiotherapy Fund at Velindre Cancer Centre. BHW receives research funding from the Medical Research Council (MRC).

Contributor Information

Kieran G Foley, Email: foleykg@cardiff.ac.uk, Division of Cancer & Genetics, School of Medicine, Cardiff University, Cardiff, UK .

Zena Riddell, Email: Zena.Riddell@wales.nhs.uk, National Imaging Academy of Wales (NIAW), Pencoed, UK .

Bernadette Coles, Email: ColesBM@cardiff.ac.uk, Velindre University NHS Trust Library & Knowledge Service, Cardiff, UK .

S Ashley Roberts, Email: Ashley.Roberts@wales.nhs.uk, Department of Clinical Radiology, University Hospital of Wales, Cardiff, UK .

Brian H Willis, Email: B.H.Willis@bham.ac.uk, Institute of Applied Health Research, University of Birmingham, Birmingham, UK .

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