Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement

Academia and Clinic18 August 2009Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA StatementFREEDavid Moher, PhD, Alessandro Liberati, MD, DrPH, Jennifer Tetzlaff, BSc, and Douglas G. Altman, DSc, the PRISMA Group*David Moher, PhDFrom Ottawa Methods Centre, Ottawa Hospital Research Institute, University of Ottawa, Ottawa, Ontario, Canada; Università di Modena e Reggio Emilia, Modena, Italy; Centro Cochrane Italiano, Istituto Ricerche Farmacologiche Mario Negri, Milan, Italy; and Centre for Statistics in Medicine, University of Oxford, Oxford, United Kingdom.Search for more papers by this author, Alessandro Liberati, MD, DrPHFrom Ottawa Methods Centre, Ottawa Hospital Research Institute, University of Ottawa, Ottawa, Ontario, Canada; Università di Modena e Reggio Emilia, Modena, Italy; Centro Cochrane Italiano, Istituto Ricerche Farmacologiche Mario Negri, Milan, Italy; and Centre for Statistics in Medicine, University of Oxford, Oxford, United Kingdom.Search for more papers by this author, Jennifer Tetzlaff, BScFrom Ottawa Methods Centre, Ottawa Hospital Research Institute, University of Ottawa, Ottawa, Ontario, Canada; Università di Modena e Reggio Emilia, Modena, Italy; Centro Cochrane Italiano, Istituto Ricerche Farmacologiche Mario Negri, Milan, Italy; and Centre for Statistics in Medicine, University of Oxford, Oxford, United Kingdom.Search for more papers by this author, and Douglas G. Altman, DScFrom Ottawa Methods Centre, Ottawa Hospital Research Institute, University of Ottawa, Ottawa, Ontario, Canada; Università di Modena e Reggio Emilia, Modena, Italy; Centro Cochrane Italiano, Istituto Ricerche Farmacologiche Mario Negri, Milan, Italy; and Centre for Statistics in Medicine, University of Oxford, Oxford, United Kingdom.Search for more papers by this author, the PRISMA Group*Search for more papers by this authorAuthor, Article, and Disclosure Informationhttps://doi.org/10.7326/0003-4819-151-4-200908180-00135 SectionsSupplemental MaterialAboutVisual AbstractPDF ToolsAdd to favoritesDownload CitationsTrack CitationsPermissions ShareFacebookTwitterLinkedInRedditEmail Editor's Note: In order to encourage dissemination of the PRISMA Statement, this article is freely accessible on the Annals of Internal Medicine Web site (www.annals.org) and will be also published in PLOS Medicine, BMJ, Journal of Clinical Epidemiology, and Open Medicine. The authors jointly hold the copyright of this article. For details on further use, see the PRISMA Web site (www.prisma-statement.org).Systematic reviews and meta-analyses have become increasingly important in health care. Clinicians read them to keep up to date with their field (1, 2), and they are often used as a starting point for developing clinical practice guidelines. Granting agencies may require a systematic review to ensure there is justification for further research (3), and some health care journals are moving in this direction (4). As with all research, the value of a systematic review depends on what was done, what was found, and the clarity of reporting. As with other publications, the reporting quality of systematic reviews varies, limiting readers' ability to assess the strengths and weaknesses of those reviews.Several early studies evaluated the quality of review reports. In 1987, Mulrow examined 50 review articles published in four leading medical journals in 1985 and 1986 and found that none met all eight explicit scientific criteria, such as a quality assessment of included studies (5). In 1987, Sacks and colleagues (6) evaluated the adequacy of reporting of 83 meta-analyses on 23 characteristics in six domains. Reporting was generally poor; between one and 14 characteristics were adequately reported (mean = 7.7; standard deviation = 2.7). A 1996 update of this study found little improvement (7).In 1996, to address the suboptimal reporting of meta-analyses, an international group developed a guidance called the QUOROM Statement (QUality Of Reporting Of Meta-analyses), which focused on the reporting of meta-analyses of randomized, controlled trials (8). In this article, we summarize a revision of these guidelines, renamed PRISMA (Preferred Reporting Items for Systematic reviews and Meta-Analyses), which have been updated to address several conceptual and practical advances in the science of systematic reviews (Box 1).Box 1. Conceptual Issues in the Evolution From QUOROM to PRISMA Download figure Download PowerPoint TerminologyThe terminology used to describe a systematic review and meta-analysis has evolved over time. One reason for changing the name from QUOROM to PRISMA was the desire to encompass both systematic reviews and meta-analyses. We have adopted the definitions used by the Cochrane Collaboration (9). A systematic review is a review of a clearly formulated question that uses systematic and explicit methods to identify, select, and critically appraise relevant research, and to collect and analyze data from the studies that are included in the review. Statistical methods (meta-analysis) may or may not be used to analyze and summarize the results of the included studies. Meta-analysis refers to the use of statistical techniques in a systematic review to integrate the results of included studies.Developing the PRISMA StatementA three-day meeting was held in Ottawa, Ontario, Canada, in June 2005 with 29 participants, including review authors, methodologists, clinicians, medical editors, and a consumer. The objective of the Ottawa meeting was to revise and expand the QUOROM checklist and flow diagram, as needed.The executive committee completed the following tasks, prior to the meeting: a systematic review of studies examining the quality of reporting of systematic reviews, and a comprehensive literature search to identify methodological and other articles that might inform the meeting, especially in relation to modifying checklist items. An international survey of review authors, consumers, and groups commissioning or using systematic reviews and meta-analyses was completed, including the International Network of Agencies for Health Technology Assessment (INAHTA) and the Guidelines International Network (GIN). The survey aimed to ascertain views of QUOROM, including the merits of the existing checklist items. The results of these activities were presented during the meeting and are summarized on the PRISMA Web site (www.prisma-statement.org).Only items deemed essential were retained or added to the checklist. Some additional items are nevertheless desirable, and review authors should include these, if relevant (10). For example, it is useful to indicate whether the systematic review is an update (11) of a previous review, and to describe any changes in procedures from those described in the original protocol.Shortly after the meeting a draft of the PRISMA checklist was circulated to the group, including those invited to the meeting but unable to attend. A disposition file was created containing comments and revisions from each respondent, and the checklist was subsequently revised 11 times. The group approved the checklist, flow diagram, and this summary paper.Although no direct evidence was found to support retaining or adding some items, evidence from other domains was believed to be relevant. For example, Item 5 asks authors to provide registration information about the systematic review, including a registration number, if available. Although systematic review registration is not yet widely available (12, 13), the participating journals of the International Committee of Medical Journal Editors (ICMJE) (14) now require all clinical trials to be registered in an effort to increase transparency and accountability (15). Those aspects are also likely to benefit systematic reviewers, possibly reducing the risk of an excessive number of reviews addressing the same question (16, 17) and providing greater transparency when updating systematic reviews.The PRISMA StatementThe PRISMA Statement consists of a 27-item checklist (Table 1; see also Table S1, for a downloadable Word template for researchers to re-use) and a four-phase flow diagram (Figure 1; see also Figure S1, for a downloadable Word template for researchers to re-use). The aim of the PRISMA Statement is to help authors improve the reporting of systematic reviews and meta-analyses. We have focused on randomized trials, but PRISMA can also be used as a basis for reporting systematic reviews of other types of research, particularly evaluations of interventions. PRISMA may also be useful for critical appraisal of published systematic reviews. However, the PRISMA checklist is not a quality assessment instrument to gauge the quality of a systematic review.Table 1. Checklist of Items to Include When Reporting a Systematic Review or Meta-AnalysisFigure 1. Flow of information through the different phases of a systematic review. Download figure Download PowerPoint From QUOROM to PRISMAThe new PRISMA checklist differs in several respects from the QUOROM checklist, and the substantive specific changes are highlighted in Table 2. Generally, the PRISMA checklist “decouples” several items present in the QUOROM checklist and, where applicable, several checklist items are linked to improve consistency across the systematic review report.Table 2. Substantive Specific Changes Between the QUOROM Checklist and the PRISMA ChecklistThe flow diagram has also been modified. Before including studies and providing reasons for excluding others, the review team must first search the literature. This search results in records. Once these records have been screened and eligibility criteria applied, a smaller number of articles will remain. The number of included articles might be smaller (or larger) than the number of studies, because articles may report on multiple studies and results from a particular study may be published in several articles. To capture this information, the PRISMA flow diagram now requests information on these phases of the review process.EndorsementThe PRISMA Statement should replace the QUOROM Statement for those journals that have endorsed QUOROM. We hope that other journals will support PRISMA; they can do so by registering on the PRISMA Web site. To underscore to authors, and others, the importance of transparent reporting of systematic reviews, we encourage supporting journals to reference the PRISMA Statement and include the PRISMA Web address in their instructions to authors. We also invite editorial organizations to consider endorsing PRISMA and encourage authors to adhere to its principles.The PRISMA Explanation and Elaboration PaperIn addition to the PRISMA Statement, a supporting Explanation and Elaboration document has been produced (18) following the style used for other reporting guidelines (19–21). The process of completing this document included developing a large database of exemplars to highlight how best to report each checklist item, and identifying a comprehensive evidence base to support the inclusion of each checklist item. The Explanation and Elaboration document was completed after several face-to-face meetings and numerous iterations among several meeting participants, after which it was shared with the whole group for additional revisions and final approval. Finally, the group formed a dissemination subcommittee to help disseminate and implement PRISMA.DiscussionThe quality of reporting of systematic reviews is still not optimal (22–27). In a recent review of 300 systematic reviews, few authors reported assessing possible publication bias (22), even though there is overwhelming evidence both for its existence (28) and its impact on the results of systematic reviews (29). Even when the possibility of publication bias is assessed, there is no guarantee that systematic reviewers have assessed or interpreted it appropriately (30). Although the absence of reporting such an assessment does not necessarily indicate that it was not done, reporting an assessment of possible publication bias is likely to be a marker of the thoroughness of the conduct of the systematic review.Several approaches have been developed to conduct systematic reviews on a broader array of questions. For example, systematic reviews are now conducted to investigate cost-effectiveness (31), diagnostic (32) or prognostic questions (33), genetic associations (34), and policy making (35). The general concepts and topics covered by PRISMA are all relevant to any systematic review, not just those whose objective is to summarize the benefits and harms of a health care intervention. However, some modifications of the checklist items or flow diagram will be necessary in particular circumstances. For example, assessing the risk of bias is a key concept, but the items used to assess this in a diagnostic review are likely to focus on issues such as the spectrum of patients and the verification of disease status, which differ from reviews of interventions. The flow diagram will also need adjustments when reporting individual patient data meta-analysis (36).We have developed an explanatory document (18) to increase the usefulness of PRISMA. For each checklist item, this document contains an example of good reporting, a rationale for its inclusion, and supporting evidence, including references, whenever possible. We believe this document will also serve as a useful resource for those teaching systematic review methodology. We encourage journals to include reference to the explanatory document in their Instructions to Authors.Like any evidence-based endeavor, PRISMA is a living document. To this end we invite readers to comment on the revised version, particularly the new checklist and flow diagram, through the PRISMA Web site. We will use such information to inform PRISMA's continued development.References1. Oxman AD, Cook DJ, Guyatt GH. Users' guides to the medical literature. VI. How to use an overview. Evidence-Based Medicine Working Group. JAMA. 1994;272:1367-71. [PMID: 7933399] CrossrefMedlineGoogle Scholar2. Swingler GH, Volmink J, Ioannidis JP. Number of published systematic reviews and global burden of disease: database analysis. BMJ. 2003;327:1083-4. [PMID: 14604930] CrossrefMedlineGoogle Scholar3. Canadian Institutes of Health Research. Randomized controlled trials registration/application checklist. December 2006. Accessed at www.cihr-irsc.gc.ca/e/documents/rct_reg_e.pdf on 19 May 2009. Google Scholar4. Young C, Horton R. Putting clinical trials into context. Lancet. 2005;366:107-8. [PMID: 16005318] CrossrefMedlineGoogle Scholar5. Mulrow CD. The medical review article: state of the science. Ann Intern Med. 1987;106:485-8. [PMID: 3813259] LinkGoogle Scholar6. Sacks HS, Berrier J, Reitman D, Ancona-Berk VA, Chalmers TC. Meta-analyses of randomized controlled trials. N Engl J Med. 1987;316:450-5. [PMID: 3807986] CrossrefMedlineGoogle Scholar7. Sacks HS, Reitman D, Pagano D, Kupelnick B. Meta-analysis: an update. Mt Sinai J Med. 1996;63:216-24. [PMID: 8692168] MedlineGoogle Scholar8. Moher D, Cook DJ, Eastwood S, Olkin I, Rennie D, Stroup DF. Improving the quality of reports of meta-analyses of randomised controlled trials: the QUOROM statement. Quality of Reporting of Meta-analyses. Lancet. 1999;354:1896-900. [PMID: 10584742] CrossrefMedlineGoogle Scholar9. Green S, Higgins J, eds. Glossary. In: Cochrane Handbook for Systematic Reviews of Interventions 4.2.5. The Cochrane Collaboration; 2005. Accessed at www.cochrane.org/resources/glossary.htm on 19 May 2009. Google Scholar10. Strech D, Tilburt J. Value judgments in the analysis and synthesis of evidence. J Clin Epidemiol. 2008;61:521-4. [PMID: 18471654] CrossrefMedlineGoogle Scholar11. Moher D, Tsertsvadze A. Systematic reviews: when is an update an update? Lancet. 2006;367:881-3. [PMID: 16546523] CrossrefMedlineGoogle Scholar12. University of York Centre for Reviews and Dissemination. 2009. Accessed at www.york.ac.uk/inst/crd/ on 19 May 2009. Google Scholar13. The Joanna Briggs Institute protocols & work in progress. 2009. Accessed at www.joannabriggs.edu.au/pubs/systematic_reviews_prot.php on 19 May 2009. Google Scholar14. De Angelis C, Drazen JM, Frizelle FA, Haug C, Hoey J, Horton R, et al; International Committee of Medical Journal Editors. Clinical trial registration: a statement from the International Committee of Medical Journal Editors [Editorial]. CMAJ. 2004;171:606-7. [PMID: 15367465] CrossrefMedlineGoogle Scholar15. Whittington CJ, Kendall T, Fonagy P, Cottrell D, Cotgrove A, Boddington E. Selective serotonin reuptake inhibitors in childhood depression: systematic review of published versus unpublished data. Lancet. 2004;363:1341-5. [PMID: 15110490] CrossrefMedlineGoogle Scholar16. Bagshaw SM, McAlister FA, Manns BJ, Ghali WA. Acetylcysteine in the prevention of contrast-induced nephropathy: a case study of the pitfalls in the evolution of evidence. Arch Intern Med. 2006;166:161-6. [PMID: 16432083] CrossrefMedlineGoogle Scholar17. Biondi-Zoccai GG, Lotrionte M, Abbate A, Testa L, Remigi E, Burzotta F, et al. Compliance with QUOROM and quality of reporting of overlapping meta-analyses on the role of acetylcysteine in the prevention of contrast associated nephropathy: case study. BMJ. 2006;332:202-9. [PMID: 16415336] CrossrefMedlineGoogle Scholar18. Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche P, Ioannidis JP, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. Ann Intern Med. 2009;151:W-65-94. LinkGoogle Scholar19. Altman DG, Schulz KF, Moher D, Egger M, Davidoff F, Elbourne D, et al; CONSORT GROUP (Consolidated Standards of Reporting Trials). The revised CONSORT statement for reporting randomized trials: explanation and elaboration. Ann Intern Med. 2001;134:663-94. [PMID: 11304107] LinkGoogle Scholar20. Bossuyt PM, Reitsma JB, Bruns DE, Gatsonis CA, Glasziou PP, Irwig LM, et al; Standards for Reporting of Diagnostic Accuracy. The STARD statement for reporting studies of diagnostic accuracy: explanation and elaboration. Ann Intern Med. 2003;138:W1-12. [PMID: 12513067] LinkGoogle Scholar21. Vandenbroucke JP, von Elm E, Altman DG, Gøtzsche PC, Mulrow CD, Pocock SJ, et al; STROBE Initiative. Strengthening the Reporting of Observational Studies in Epidemiology (STROBE): explanation and elaboration. Ann Intern Med. 2007;147:W163-94. [PMID: 17938389] LinkGoogle Scholar22. Moher D, Tetzlaff J, Tricco AC, Sampson M, Altman DG. Epidemiology and reporting characteristics of systematic reviews. PLoS Med. 2007;4:78. [PMID: 17388659] CrossrefMedlineGoogle Scholar23. Bhandari M, Morrow F, Kulkarni AV, Tornetta P. Meta-analyses in orthopaedic surgery. A systematic review of their methodologies. J Bone Joint Surg Am. 2001;83-A:15-24. [PMID: 11205853] CrossrefMedlineGoogle Scholar24. Kelly KD, Travers A, Dorgan M, Slater L, Rowe BH. Evaluating the quality of systematic reviews in the emergency medicine literature. Ann Emerg Med. 2001;38:518-26. [PMID: 11679863] CrossrefMedlineGoogle Scholar25. Richards D. The quality of systematic reviews in dentistry. Evid Based Dent. 2004;5:17. [PMID: 15238972] CrossrefMedlineGoogle Scholar26. Choi PT, Halpern SH, Malik N, Jadad AR, Tramèr MR, Walder B. Examining the evidence in anesthesia literature: a critical appraisal of systematic reviews. Anesth Analg. 2001;92:700-9. [PMID: 11226105] CrossrefMedlineGoogle Scholar27. Delaney A, Bagshaw SM, Ferland A, Manns B, Laupland KB, Doig CJ. A systematic evaluation of the quality of meta-analyses in the critical care literature. Crit Care. 2005;9:R575-82. [PMID: 16277721] CrossrefMedlineGoogle Scholar28. Dickersin K. Publication bias: recognizing the problem, understanding its origins and scope, and preventing harm.. In: Rothstein HR, Sutton AJ, Borenstein M, eds. Publication Bias in Meta-Analysis—Prevention, Assessment and Adjustments. Chichester, UK: J Wiley; 2005:11-33. Google Scholar29. Sutton AJ. Evidence concerning the consequences of publication and related biases.. In: Rothstein HR, Sutton AJ, Borenstein M, eds. Publication Bias in Meta-Analysis—Prevention, Assessment and Adjustments. Chichester, UK: J Wiley; 2005:175-92. Google Scholar30. Lau J, Ioannidis JP, Terrin N, Schmid CH, Olkin I. The case of the misleading funnel plot. BMJ. 2006;333:597-600. [PMID: 16974018] CrossrefMedlineGoogle Scholar31. Ladabaum U, Chopra CL, Huang G, Scheiman JM, Chernew ME, Fendrick AM. Aspirin as an adjunct to screening for prevention of sporadic colorectal cancer. A cost-effectiveness analysis. Ann Intern Med. 2001;135:769-81. [PMID: 11694102] LinkGoogle Scholar32. Deeks JJ. Systematic reviews in health care: Systematic reviews of evaluations of diagnostic and screening tests. BMJ. 2001;323:157-62. [PMID: 11463691] CrossrefMedlineGoogle Scholar33. Altman DG. Systematic reviews of evaluations of prognostic variables. BMJ. 2001;323:224-8. [PMID: 11473921] CrossrefMedlineGoogle Scholar34. Ioannidis JP, Ntzani EE, Trikalinos TA, Contopoulos-Ioannidis DG. Replication validity of genetic association studies. Nat Genet. 2001;29:306-9. [PMID: 11600885] CrossrefMedlineGoogle J, Oxman A, E. systematic reviews that inform health care and J Health [PMID: CrossrefMedlineGoogle of meta-analyses using updated individual patient data. Cochrane Working Group. Med. [PMID: CrossrefMedlineGoogle E, R, I, L, Liberati A. Assessment of methodological quality of studies by systematic reviews: results of the study. BMJ. [PMID: CrossrefMedlineGoogle Guyatt GH, Oxman AD, R, P, et al; Working Group. an on quality of evidence and of BMJ. [PMID: CrossrefMedlineGoogle R, Cook DJ, A, et al; and An the quality of evidence and of in guidelines and J Crit Med. [PMID: CrossrefMedlineGoogle A, Gøtzsche PC, Altman DG. evidence for reporting of in randomized trials: of protocols to published articles. JAMA. [PMID: CrossrefMedlineGoogle Schmid I, Altman DG. reporting bias in randomized trials by the Canadian Institutes of Health Research. CMAJ. [PMID: CrossrefMedlineGoogle CA, P, protocols of systematic reviews: what was to what was JAMA. [PMID: CrossrefMedlineGoogle In to A Article, and Disclosure From Ottawa Methods Centre, Ottawa Hospital Research Institute, University of Ottawa, Ottawa, Ontario, Canada; Università di Modena e Reggio Emilia, Modena, Italy; Centro Cochrane Italiano, Istituto Ricerche Farmacologiche Mario Negri, Milan, Italy; and Centre for Statistics in Medicine, University of Oxford, Oxford, United The following to the PRISMA Altman, DSc, Centre for Statistics in Medicine United PhD, University Hospital MD, Health Research & Health PLoS Medicine United PhD, Hospital of Ontario, A. & Research and PhD, PLoS Medicine the of United PhD, Cochrane Centre United and of and MD, of Medicine, Clinical Epidemiology and University Ontario, PhD, Università di Modena e Reggio and Centro Cochrane Italiano, Istituto Ricerche Farmacologiche Mario J. PhD, University of United MD, PhD, of Medicine, Clinical Epidemiology and University Ontario, PhD, of Health MD, of and Medicine, University of MD, PhD, Medical United MD, The Cochrane Centre PhD, Ottawa Hospital Research Institute Ontario, MD, of Medicine, Clinical Epidemiology and University Ontario, PhD, United MD, University of MD, PhD, Systematic Reviews United and for Health and University of the and Alessandro Liberati, MD, Università di Modena e Reggio and Centro Cochrane Italiano, Istituto Ricerche Farmacologiche Mario MD, Centre for the of the of Health PhD, The United MD, Centro Cochrane Italiano, Istituto Ricerche Farmacologiche Mario Moher, PhD, Ottawa Methods Centre, Ottawa Hospital Research Institute Ontario, MD, Annals of Internal Medicine for Medical MD, Health Research Centre Health and Technology Assessment Ontario, Canada; at the of the first meeting of the group, Ontario, MD, University of Hospital of Ontario, PhD, Health International G. MD, PhD, Evidence-Based Jennifer Tetzlaff, BSc, Ottawa Methods Centre, Ottawa Hospital Research Institute Ontario, The Cochrane Cochrane Collaboration United at the of the first meeting of the group, United and MD, Institute of University of Ottawa Ontario, PRISMA was by the Canadian Institutes of Health Università di Modena e Reggio Emilia, Italy; Research Clinical Evidence The Cochrane Collaboration; and Liberati is in through of the of University and Altman is by Research Moher is by a University of Ottawa Research of the any in the or of the PRISMA no a role in the Moher, PhD, Ottawa Methods Centre, Ottawa Hospital Research Institute, The Ottawa Ottawa, Canada; Moher and Ottawa Methods Centre, Ottawa Hospital Research Institute, The Ottawa Ottawa, Università di Modena e Reggio and Centro Cochrane Italiano, Istituto Ricerche Farmacologiche Mario Negri, Milan, Centre for Statistics in Medicine, University of Oxford, United of the PRISMA is in the PRISMA Statement for Reporting Systematic Reviews and of Studies Health Explanation and Elaboration Alessandro Liberati Douglas G. Altman Jennifer