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The appropriateness of asymmetry tests for publication bias in meta-analyses: a large survey
Open accessAbstract
BACKGROUND: Statistical tests for funnel-plot asymmetry are common in meta-analyses. Inappropriate application can generate misleading inferences about publication bias. We aimed to measure, in a survey of meta-analyses, how frequently the application of these tests would be not meaningful or inappropriate. METHODS: We evaluated all meta-analyses of binary outcomes with é 3 studies in the Cochrane Database of Systematic Reviews (2003, issue 2). A separate, restricted analysis was confined to the largest meta-analysis in each of the review articles. In each meta-analysis, we assessed whether criteria to apply asymmetry tests were met: no significant heterogeneity, I2 < 50%, é 10 studies (with statistically significant results in at least 1) and ratio of the maximal to minimal variance across studies > 4. We performed a correlation and 2 regression asymmetry tests and evaluated their concordance. Finally, we sampled 60 meta-analyses from print journals in 2005 that cited use of the standard regression test. RESULTS: A total of 366 of 6873 (5%) and 98 of 846 meta-analyses (12%) in the wider and restricted Cochrane data set, respectively, would have qualified for use of asymmetry tests. Asymmetry test results were significant in 7%-18% of the meta-analyses. Concordance between the 3 tests was modest (estimated k 0.33-0.66). Of the 60 journal meta-analyses, 7 (12%) would qualify for asymmetry tests; all 11 claims for identification of publication bias were made in the face of large and significant heterogeneity. INTERPRETATION: Statistical conditions for employing asymmetry tests for publication bias are absent from most meta-analyses; yet, in medical journals these tests are performed often and interpreted erroneously.
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“However, publication bias tests might be problematic for IN-OT studies due to small sample sizes resulting in insufficient statistical power and sample size variability for the tests to yield reliable and significant results (26).”
From Statistical and Methodological Considerations for the Interpretation of Intranasal Oxytocin Studies (2016) · cites this paper as [26]
Experimental — accuracy not yet measuredIn the citing paper
“The small number of studies and presence of significant heterogeneity precluded formal testing for publication bias[35].”
From Daily Sitting Time and All-Cause Mortality: A Meta-Analysis (2013) · cites this paper as [35]
In the citing paper
“Of 60 meta-analyses in 24 articles published in 2005 in which formal assessments were reported, most were based on fewer than ten studies; most displayed statistically significant heterogeneity; and many reviewers misinterpreted the results of the tests employed [123].”
From The PRISMA Statement for Reporting Systematic Reviews and Meta-Analyses of Studies That Evaluate Health Care Interventions: Explanation and Elaboration (2009) · cites this paper as [123]
In the citing paper
“Although evidence that smaller studies had larger estimated effects than large ones may suggest the possibility that the available evidence is biased, misinterpretation of such data is common [123].”
From The PRISMA Statement for Reporting Systematic Reviews and Meta-Analyses of Studies That Evaluate Health Care Interventions: Explanation and Elaboration (2009) · cites this paper as [123]
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“Egger’s test was used to investigate the presence of publication bias.(19) The recommendations of the International Ankle Consortium were used to further assess between-study variability in patients with CAI.”
MethodSystematic review evaluating cardiovascular events of the 5-alpha reductase inhibitor - Dutasteride
Loke, Y. K., Ho, R., Smith, M., Wong, O., Sandhu, M. S., Sage, W., & Singh, S. (2013) · Journal of Clinical Pharmacy and Therapeutics · doi:10.1111/jcpt.12080 · Cited by 27
“Funnel plots were used to assess publication bias.(9) In studies with multiple arms, we preferentially chose to analyse data based on the dutasteride vs.”
MethodTharabenjasin, P., Pabalan, N., & Jarjanazi, H. (2019) · PLoS ONE · doi:10.1371/journal.pone.0200967 · Cited by 29
Febuxostat administration for the prevention of tumour lysis syndrome: A meta‐analysis
Bellos, I., Kontzoglou, K., Psyrri, A. K., & Pergialiotis, V. (2019) · Journal of Clinical Pharmacy and Therapeutics · doi:10.1111/jcpt.12839 · Cited by 27
Oostra, E., Jażdżyk, P., Vis, V., Dalhuisen, I., Hoogendoorn, A. W., Planting, C. H. M., van Eijndhoven, P., van der Werf, Y. D., van den Heuvel, O. A., & van Exel, E. R. (2024) · Acta Psychiatrica Scandinavica · doi:10.1111/acps.13768 · Cited by 30
“119 In addition, Dal-huisen et al. (2022) 9 suggested with their meta-regression that the significant tests for publication bias are the results of substantial heterogeneity instead of publication bias.”
Electrosurgical bipolar vessel sealing for vaginal hysterectomies
Pergialiotis, V., Vlachos, D., Rodolakis, A., Haidopoulos, D. A., Christakis, D., & Vlachos, G. D. (2014) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-014-3238-0 · Cited by 26
“Publication bias was not assessed due to the small number of studies included in the present meta-analysis [6].”
BackgroundEfficacy and adverse effects of collagenase use in the treatment of Dupuytren’s disease
Sanjuán-Cerveró, R., Carrera‐Hueso, F. J., Vazquez‐Ferreiro, P., & Barrios, M. A. R. (2018) · The Bone & Joint Journal · doi:10.1302/0301-620x.100b1.bjj-2017-0463.r1 · Cited by 26
Weekend effect in acute coronary syndrome: A meta-analysis of observational studies
Kwok, C. S., Al-Dokheal, M., Aldaham, S. A., Rushton, C. A., Butler, R., Kinnaird, T. D., Zaman, A., Zaman, M., Timmis, A., & Mamas, M. A. (2018) · European Heart Journal Acute Cardiovascular Care · doi:10.1177/2048872618762634 · Cited by 26
Wilhelm, B., Waddell, L. A., Greig, J. D., & Young, I. (2019) · PLoS ONE · doi:10.1371/journal.pone.0216826 · Cited by 28
Pabalan, N., Tharabenjasin, P., Suntornsaratoon, P., Jarjanazi, H., & Muanprasat, C. (2020) · Infection Genetics and Evolution · doi:10.1016/j.meegid.2020.104682 · Cited by 26
“Publication bias was considered for comparisons that met two conditions: (i) ≥ 10 studies only (Ioannidis and Trikalinos, 2007) and (ii) significant outcomes.”
de Miranda, J. P., Silva, W. T., Silva, H. J., Mascarenhas, R. O., & Oliveira, V. C. (2021) · Physical Therapy in Sport · doi:10.1016/j.ptsp.2021.03.011 · Cited by 26
Xiong, L., Gong, S., Lu, T., Tian, H., Miao, C., Liu, L., Jiang, Z.-L., Hao, J., Jing, K., Yang, K., et al. (2022) · Journal of Gastrointestinal Surgery · doi:10.1007/s11605-022-05304-1 · Cited by 26
Small Study Effects in Diagnostic Imaging Accuracy
Lu, L., Phua, Q. S., Bacchi, S., Goh, R., Gupta, A. K., Kovoor, J. G., Ovenden, C. D., & To, M. (2022) · JAMA Network Open · doi:10.1001/jamanetworkopen.2022.28776 · Cited by 29
“Of these primary studies, the smallest trial included 5 participants; the largest, 3200 participants; there was a mean (SD) of 122 (186) participants and median (IQR) of 80 (46-137) participants per study.”
Glasziou, P., Chalmers, I., Altman, D. G., Bastian, H., Boutron, I., Brice, A., Jamtvedt, G., Farmer, A. A., Ghersi, D., Groves, T., et al. (2010) · Cited by 26
Use of “big data” in drug discovery and clinical trials
Taglang, G., & Jackson, D. (2016) · Gynecologic Oncology · doi:10.1016/j.ygyno.2016.02.022 · Cited by 26
Examining and Interpreting Doi Plot Asymmetry in Meta‐Analyses of Randomized Controlled Trials
Furuya‐Kanamori, L., Rousou, X., Kostoulas, P., & Doi, S. A. R. (2025) · Journal of Evidence-Based Medicine · doi:10.1111/jebm.70063 · Cited by 30
The Sutton Trust-Education Endowment Foundation Teaching and Learning Toolkit: Technical Appendices
Higgins, S., Katsipataki, M., & Coe, R. (2013) · Cited by 25
Long, B., Yu, Z., Zhou, H., Ma, Z., Ren, Y., Zhan, H., Li, L., Cao, H., & Jiao, Z. (2018) · International Journal of Surgery · doi:10.1016/j.ijsu.2018.06.033 · Cited by 25
Leite, H. R., Camargos, A. C. R., Mendonça, V. A., Lacerda, A. C. R., Soares, B. A., & Oliveira, V. C. (2018) · Brazilian Journal of Physical Therapy · doi:10.1016/j.bjpt.2018.09.005 · Cited by 27
Papageorgiou, S. N., Papadopoulos, M. A. A. P., & Athanasiou, A. E. (2014) · Clinical Oral Investigations · doi:10.1007/s00784-014-1196-3 · Cited by 27
“10 [24, 29].”
Cao, D.-H., Gu, W.-B., Zhao, H.-Y., Hu, J.-L., & Yuan, H. (2024) · Archives of Osteoporosis · doi:10.1007/s11657-024-01400-8 · Cited by 25
“Inter-study inconsistency was quantified by , where Q is the chi-square statistic and df is its degree of freedom [14–16].”
Ingram, L. A., Tomkinson, G. R., d’Unienville, N. M. A., Gower, B., Gleadhill, S., Boyle, T., & Bennett, H. (2025) · Sports Medicine · doi:10.1007/s40279-025-02204-7 · Cited by 27
“…considerable heterogeneity) [60]; (iii) indirectness if there were significant differences in populations, outcomes or interventions used between studies; (iv) imprecision if data from < 800 participants per outcome were analysed [61, 62]; and (v) publication bias if Egger’s test was significant.”
Tan, S. K., Leung, W. K., Tang, A. T. H., & Zwahlen, R. A. (2017) · PLoS ONE · doi:10.1371/journal.pone.0181146 · Cited by 24
“Funnel plot was used to assess publication bias, while Egger test for funnel plot asymmetry will be used when more than ten primary studies were included in an analysis[23, 24].”
Yee, J., Kim, S. M., Han, J., Lee, N., Yoon, H. Y., & Gwak, H. S. (2020) · Scientific Reports · doi:10.1038/s41598-020-60467-8 · Cited by 24
Manicone, P. F., Angelis, P. D., Rella, E., Damis, G., & D’Addona, A. (2021) · Journal of Prosthetic Dentistry · doi:10.1016/j.prosdent.2020.11.042 · Cited by 24
da Rocha, T. J. C. M., Melson, E., Zamora, J., Fernandez-Felix, B. M., Arlt, W., & Thangaratinam, S. (2023) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgad599 · Cited by 24
Metadata
- Authors
- Ioannidis, J. P. A., & Trikalinos, T. A.
- Affiliations
- Tufts University (US)
- Venue
- Canadian Medical Association Journal
- Publisher
- CMA Joule Inc.
- Published
- 2007-04-10
- Volume
- 176
- Issue
- 8
- Pages
- 1091-1096
- ISSN
- 0820-3946 (ISSN-L)
- 1488-2329
- PMC
- PMC1839799
- OpenAlex
- W2164093802
- Cited by
- 1,052
- References
- 40
- Citations by year
- 2026: 49 · 2025: 48 · 2024: 64 · 2023: 49 · 2022: 81 · 2021: 73 · 2020: 83 · 2019: 81 · 2018: 73 · 2017: 55 · 2016: 62 · 2015: 64 · 2014: 68 · 2013: 38 · 2012: 39
- FWCI
- 31.66
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Canadian Medical Association Journal (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Social Sciences › Decision Sciences › Statistics, Probability and Uncertainty › Meta-analysis and systematic reviews
- Physical Sciences › Mathematics › Statistics and Probability › Statistical Methods in Epidemiology
- Social Sciences › Library and Information Sciences › scientometrics and bibliometrics research
- Keywords
- publication bias, funnel plot asymmetry, meta-analysis, heterogeneity, Cochrane Database of Systematic Reviews, binary outcomes, test concordance
- MeSH terms
- Data Interpretation, Statistical, Humans, Periodicals as Topic, Meta-Analysis as Topic, Databases, Bibliographic, Publication Bias
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