Does the medical literature remain inadequately described despite having reporting guidelines for 21 years? &ndash; A systematic review of reviews: an update

Yanling Jin; Nitika Sanger; Ieta Shams; Candice Luo; Hamnah Shahid; Guowei Li; Meha Bhatt; Laura Zielinski; Bianca Bantoto; Mei Wang; Luciana PF Abbade; Ikunna Nwosu; Alvin Leenus; Lawrence Mbuagbaw; Muhammad Maaz; Yaping Chang; Guangwen Sun; Mitchell AH Levine; Jonathan D Adachi; Lehana Thabane; Zainab Samaan

doi:10.2147/JMDH.S155103

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Review

Does the medical literature remain inadequately described despite having reporting guidelines for 21 years? – A systematic review of reviews: an update

Authors Jin Y , Sanger N, Shams I, Luo C, Shahid H , Li G, Bhatt M, Zielinski L , Bantoto B, Wang M , Abbade LPF , Nwosu I, Leenus A , Mbuagbaw L, Maaz M, Chang Y, Sun G, Levine MAH , Adachi JD , Thabane L, Samaan Z

Received 25 October 2017

Accepted for publication 10 April 2018

Published 27 September 2018 Volume 2018:11 Pages 495—510

DOI https://doi.org/10.2147/JMDH.S155103

Checked for plagiarism Yes

Review by Single anonymous peer review

Peer reviewer comments 2

Editor who approved publication: Dr Scott Fraser

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Yanling Jin,^1,* Nitika Sanger,^2,* Ieta Shams,^3,* Candice Luo,^4,* Hamnah Shahid,^5,* Guowei Li,^1,* Meha Bhatt,¹ Laura Zielinski,⁶ Bianca Bantoto,⁷ Mei Wang,¹ Luciana PF Abbade,⁸ Ikunna Nwosu,⁴Alvin Leenus,¹Lawrence Mbuagbaw,¹ Muhammad Maaz,¹ Yaping Chang,¹ Guangwen Sun,¹Mitchell AH Levine,^1,9 Jonathan D Adachi^1,9 Lehana Thabane,^1,9 Zainab Samaan^1,10

¹Department of Health Research Methods, Evidence and Impact, McMaster University, Hamilton, ON, Canada; ²Department of Medical Science, Medical Sciences Graduate Program, McMaster University, Hamilton, ON, Canada; ³Department of Psychology, Neuroscience and Behaviour, McMaster University, Hamilton, ON, Canada; ⁴Faculty of Health Sciences, Bachelors of Health Sciences, McMaster University, Hamilton, ON, Canada; ⁵Department of Arts and Science, McMaster University, Hamilton, ON, Canada; ⁶Department of Neuroscience, McMaster Integrative Neuroscience Discovery and Study, McMaster University, Hamilton, ON, Canada; ⁷Department of Science, Honours Integrated Sciences Program, McMaster University, Hamilton, ON, Canada; ⁸Department of Dermatology and Radiotherapy, Botucatu Medical School, Universidade Estadual Paulista, UNESP, São Paulo, Brazil; ⁹St. Joseph’s Healthcare Hamilton, Hamilton, ON, Canada; ¹⁰Department of Psychiatry and Behavioural Neurosciences, McMaster University, Hamilton, ON, Canada

^*These authors contributed equally to this work

Purpose: Reporting guidelines (eg, Consolidated Standards of Reporting Trials [CONSORT] statement) are intended to improve reporting standards and enhance the transparency and reproducibility of research findings. Despite accessibility of such guidelines, researchers are not required to adhere to them. Our goal was to determine the current status of reporting quality in the medical literature and examine whether adherence of reporting guidelines has improved since the inception of reporting guidelines.
Materials and methods: Eight reporting guidelines, such as CONSORT, Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA), STrengthening the Reporting of OBservational studies in Epidemiology (STROBE), Quality of Reporting of Meta-analysis (QUOROM), STAndards for Reporting of Diagnostic accuracy (STARD), Animal Research: Reporting In Vivo Experiments (ARRIVE), Consolidated Health Economic Evaluation Reporting Standards (CHEERS), and Meta-analysis of Observational Studies in Epidemiology (MOOSE) were examined. Our inclusion criteria included reviews published between January 1996 to September 2016 which investigated the adherence to reporting guidelines in the literature that addressed clinical trials, systematic reviews, observational studies, meta-analysis, diagnostic accuracy, economic evaluations, and preclinical animal studies that were in English. All reviews were found on Web of Science, Excerpta Medical Database (EMBASE), MEDLINE, and Cumulative Index to Nursing and Allied Health Literature (CINAHL).
Results: Among the general searching of 26,819 studies by using the designed searching method, 124 studies were included post screening. We found that 87.9% of the included studies reported suboptimal adherence to reporting guidelines. Factors associated with poor adherence included non-pharmacological interventions, year of publication, and trials concluding with significant results. Improved adherence was associated with better study designs such as allocation concealment, random sequence, large sample sizes, adequately powered studies, multiple authorships, and being published in journals endorsing guidelines.
Conclusion: We conclude that the level of adherence to reporting guidelines remains suboptimal. Endorsement of reporting guidelines by journals is important and recommended.

Keywords: guidelines, adherence, review, CONSORT

Introduction

Medical science is an evolving and dynamic field of research that impacts health care, disease outcomes, and health care systems in general. The evidence generated from millions of medical publications is meant to inform these dynamic changes and therefore has to be presented in a clear, consistent, and transparent fashion. There are more than 26 million citations for biomedical literature in the PubMed¹ database alone. To understand and evaluate the evidence presented in these citations, a harmonized method of reporting the research findings is needed to ensure clarity, consistency, and the uptake and dissemination of knowledge.² Tremendous efforts have been made to provide guidelines for different types of research designs to assist in the process of transparent and clear reporting, eg, Enhancing the QUAlity and Transparency Of health Research (EQUATOR) Network website.³ However, despite the wide availability of such guidelines since the inception of the Consolidated Standards of Reporting Trials (CONSORT⁴) statement in 1996, the uptake remains suboptimal in the face of the exponential volume of medical literature leaving the readers confused. For example, some studies show positive harmful results from eating red meat on the risk of having colorectal cancer,⁵ while others are showing inconsistent effect marked by substantial methodological differences, type of red meat investigated, and the population selection limitations.⁶ Therefore, the reader is unable to decide whether red meat has an effect on bowel cancer risk. Poor reporting without using well-designed guidelines in primary studies may lead to a bias in the treatment effects found in systematic reviews. In addition, poorly conducted systematic reviews may not be able to detect the bias effect that the studies included. In a previous study, we conducted a scoping review and examined the level of adherence to six reporting guidelines and found the level of adherence to be suboptimal in 86% of the included studies.⁷

The aim of this review was to conduct a systematic review of reviews to update the state of adherence to guidelines since 2012 and to identify factors associated with improved adherence. Our hypothesis was that the reporting standards have improved since our last examination in 2012 given that a longer period has passed after guideline statements were first introduced for researchers and more journals started to endorse the guidelines. Our search was looking at reviews published between January 1, 1996, and September 30, 2016.

Materials and methods

This systematic review was performed and reported according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines.⁸ A protocol for a series of three reviews including the current systematic review has been peer reviewed and published elsewhere.⁹

Study inclusion and exclusion criteria

Systematic reviews which investigated the adherence to commonly used reporting guidelines in medical literature that addressed clinical trials, systematic reviews, observational studies, meta-analysis, diagnostic accuracy, economic evaluations, and preclinical animal studies that have been reported in English were selected. Eight guidelines included in this review were as follows: CONSORT,⁴ PRISMA,⁸ STrengthening the Reporting of OBservational studies in Epidemiology (STROBE),¹⁰ Quality of Reporting of Meta-analysis (QUOROM),¹¹ STAndards for Reporting of Diagnostic accuracy (STARD),¹² Animal Research: Reporting In Vivo Experiments (ARRIVE),¹³ Consolidated Health Economic Evaluation Reporting Standards (CHEERS),¹⁴ and Meta-analysis of Observational Studies in Epidemiology (MOOSE).¹⁵

The exclusion criteria included studies that 1) were not systematic reviews; 2) did not explore adherence to the aforementioned reporting guidelines; 3) did not provide data on guideline adherence; 4) were subsets of the included studies; 5) published abstracts, letters, editorials, or commentaries; and 6) reviews in languages other than English for feasibility and resource purposes.

Search strategy

The search strategy was based on the previously published review⁷ and was updated for this systematic review. We searched four databases (Excerpta Medical Database [EMBASE], MEDLINE, Cumulative Index to Nursing, and Allied Health Literature [CINAHL], and Web of Science) from 1996 (CONSORT inception – first created guideline among all eight included guidelines) to September 30, 2016.

We used the following search terms for each of the four databases: (Systematic reviews OR reviews OR quality of reporting OR completeness of reporting) AND (CONSORT OR STROBE OR QUOROM OR PRISMA OR MOOSE OR STARD OR ARRIVE OR CHEERS) OR adherence. Detailed search terms have been reported in the published protocol.⁹ All stages of search, inclusion, exclusion, and data abstraction were performed independently in duplicate, and agreement was reached through team discussion and consensus.

Outcome measures

The primary outcome was the level of adherence to reporting guidelines and their checklists as reported in the systematic reviews. The secondary outcome included the factors that were associated with improved adherence to guidelines.

Data extraction

A specific data abstraction form was designed to include the following data: 1) general characteristics of the included studies (first author, publication year, country, journal, study field, search time frame, data sources, numbers of included primary studies, and study design), 2) main findings from the included studies, 3) authors’ summaries and conclusions, and 4) factors reported to be related to improved guideline reporting adherence. Each assessment of the systematic reviews was conducted in duplicate. Calibration was performed on the data extraction form. If the pair of evaluators was unable to come to a conclusion, a third-party reviewer would have settled the dispute.

Quality evaluation

We used the modified Assessing the Methodological Quality of Systematic Reviews/Overview of Quality Assessment Questionnaire (Assessment of Multiple Systematic Reviews [AMSTAR]/Overview Quality Assessment Questionnaire [OQAQ]), a 10-item scale,⁷ to assess the quality of the systematic reviews included in this review. We assigned a number out of a maximum of 20 points for each included study. The higher the number assigned, the better the quality of the systematic review.

Data synthesis

We provided a qualitative summary and characteristics of the included studies. We summarized the factors associated with adherence based on the included study results; no quantitative analysis was possible in this review. We also reported the percentage of studies in which the level of adherence to reporting each guideline was suboptimal. This was calculated by dividing the number of studies with this finding by the total number of studies evaluating the guideline.

Results

Our search resulted in a total of 9,123 publications, of which 124 systematic reviews that included 26,819 primary studies were included in this systematic review of reviews. Figure 1 shows the PRISMA flowchart for the included studies.

Figure 1 PRISMA flow diagram.

Abbreviation: PRISMA, Preferred Reporting Items for Systematic Reviews and Meta-Analyses.

The characteristics of the included studies are described in Table 1. The majority of the studies (65% of the total 124 included studies) investigated the adherence to the CONSORT statement as expected since it is the first and oldest guideline. The second most commonly investigated guideline is the PRISMA with 19 studies (15%; Table 1).

Table 1 Characteristics of the included studies

Abbreviations: ARRIVE, Animal Research: Reporting In Vivo Experiments; BMC, BioMed central; BMJ, British Medical Journal; CHEERS, Consolidated Health Economic Evaluation Reporting Standards; CONSORT, Consolidated Standards of Reporting Trials; International Urogyn J, International Urogynecology Journal; JAMA, The Journal of the American Medical Association; MOOSE, Meta-analysis of Observational Studies in Epidemiology; OTJR, Occupational Therapy Journal of Research; PLoS, Public Library of Science; PRISMA, Preferred Reporting Items for Systematic reviews and Meta-Analyses; QUOROM, Quality of Reporting of Meta-analysis; STARD, Standards for Reporting of Diagnostic Accuracy; STROBE, Strengthening the Reporting of Observational Studies in Epidemiology.

The majority of studies used the guideline checklist to evaluate the level of adherence and generated a mean score as summarized in Table S1. Table S1 summarizes the studies’ findings by guideline with authors’ conclusions for each study. Most studies described the adherence to the different guidelines using the following qualitative descriptors:

deficient, not adequately reported, generally poor, suboptimal, poor, medium, low, poor to moderate, lack of CONSORT adherence, bad, far from satisfactory, lack of standard reporting, improvement over the years has been minor, weak, quality of the articles varied substantially, insufficient, missed reporting some important factors, deficiencies in reporting, inconsistent, needs to be improved, inadequate, there is a need for improvement in quality of reporting, overall adherence is low.

A summary of the quantitative assessment of adherence to guidelines is presented in Table 2.

Table 2 Summary of the included studies’ conclusions

Note: ^aThe number of studies concluding that “some improvements are needed, reporting inadequate, poor, medium, suboptimal, etc.”

Abbreviations: ARRIVE, Animal Research: Reporting In Vivo Experiments; CHEERS, Consolidated Health Economic Evaluation Reporting Standards; CONSORT, Consolidated Standards of Reporting Trials; MOOSE, Meta-analysis of Observational Studies in Epidemiology; PRISMA, Preferred Reporting Items for Systematic Reviews and Meta-Analyses; QUOROM, Quality of Reporting of Meta-analysis; STARD, Standards for Reporting of Diagnostic Accuracy; STROBE, Strengthening the Reporting of Observational Studies in Epidemiology.

The level of adherence to all included reporting guidelines was 87.9% of all guidelines combined showing a need for improvement in reporting. Factors associated with poor adherence to CONSORT guideline included trials with significantly positive results, trials with the categorical outcome, trials conducted in North America compared to Europe, and trials funded by nonindustry source. A summary of factors associated with adherence standards is summarized in Table 3. Several factors were associated with better reporting standards relating to authors, study design, outcome specifications, year of publication (recent years of publications are associated with better reporting standards), journal, funding source, and study/author country.

Table 3 Factors associated with reporting quality of articles using the CONSORT guideline

Notes: ^aStatistically significant increase/decrease, p≤0.05; (↑), positively associated with adherence; (↓), negatively associated with adherence. The number of studies concluding that “some improvements are needed, reporting inadequate, poor, medium, suboptimal, etc”. ^bAssociation of Southeast Asian nations, Association of Southeast Asian Nations (ASEAN) plus six groups, which composed of the members of the ASEAN plus Australia, China, India, Japan, New Zealand, and South Korea.

Abbreviations: CONSORT, Consolidated Standards of Reporting Trials; JCEM, The Journal of Clinical Endocrinology and Metabolism; RCT, randomized control trial.

Factors associated with improved adherence to reporting guidelines

Author factors

The included studies reported that the expertise of the author team, for example, an epidemiologist, improved the quality of reporting the study. In addition, having multiple authors also improved reporting quality.

Study factors

Study design with detailed methods including allocation concealment, randomization, specific outcome measures, sample size and power calculations, acknowledgment of limitations and sources of bias, larger sample size, registration of clinical trials, pharmacological interventions, and detailed statistical analysis plan were associated with better reporting and adherence to reporting guidelines. Year of publication was also associated with adherence in which the more recently published articles had increased adherence.

Journal factor

Publications in journals endorsing reporting guidelines have better adherence to these guidelines than articles published in journals that do not endorse such guidelines. In addition, journals’ impact factor, medical journals, and journals with restriction on the number of words per article also had articles with better reporting standards. Publication in a general medical journal was associated with better reporting quality than a specialty journal.

Ethics and funding factors

Articles that reported ethical approval, participants’ consent, and the source of funding were associated with improved adherence to reporting guidelines.

Country of study factors

Geographic location of the study has an impact on the quality of reporting and adherence to reporting guidelines, for example, studies reported from Europe had better reporting standards compared to studies from North America. Studies reported from China had lower adherence to guidelines than elsewhere indicating geographical variations may directly or indirectly impact the level of adherence to reporting guidelines in the medical literature.

Quality assessment of included studies

For each included systematic review, we performed a quality assessment using the modified AMSTAR/OQAQ score. Table 4 provides the total score out of 20 for each study. The scores varied from 9 to 20. The average score for all the included studies is 16.14. The lowest scores were related to items 5 and 6 of the quality assessment related to the availability of the primary studies’ characteristics similar to a previously reported study.⁷ Items 5 and 6 were evaluated if there was information on included and excluded studies provided and if the characteristics of included studies provided, respectively.

Table 4 Reporting quality of the 124 included systematic reviews, assessed by the modified AMSTAR/OQAQ (10 items, score out of 20)

Abbreviations: AMSTAR, Assessment of Multiple Systematic Reviews; OQAQ, Overview Quality Assessment Questionnaire.

Discussion

The medical literature is paramount to the progression of the understanding of health and disease and the establishment of priorities and recommendations for prevention, diagnosis, treatment, and measurement of outcomes. To implement research findings, transparent and consistent reporting standards are needed to help make informed decisions. Such standards have been set by the CONSORT working group and others for the past 2 decades with the aim of improving the reporting standards in biomedical research. It is expected that the introduction of new change to the current practice will take time to adopt and disseminate. However, the uptake of the widely available guidelines has been less than ideal. We define suboptimal and less than ideal as <100%. The whole idea of a systematic review is to have completely transparent methods reported, so everyone can follow and reproduce the results. Inherently, systematic reviews are meant to be a more rigorous study design. This allows them to produce meaningful results than individual studies. Thus, when reviews fail to adhere to reporting guidelines, it calls into question the consistency of their results. Given the weight that systematic reviews have in the scientific community, it is imperative that we hold reviews to a high standard.

Five years ago, we investigated the level of adherence to reporting standards in the medical literature, and we identified 86% of the systematic reviews conducted on the level of adherence to reporting guidelines of the medical literature to be less than ideal.⁷ Since our previous scoping review, many new revisions and updates to reporting guidelines have been introduced. Currently, there are 358 reporting guidelines on the EQUATOR Network website¹⁶ for many study types that are freely available. However, endorsement of reporting guidelines by journals still remains low.

Among all the factors that can improve the reporting quality, such as author factors, study factors, journal factors, ethics and funding factors, and country of study factors, author factors as well as their limitations have been studied in other researches. The author factors were the number of the authors of the publication and the level of expertise in the different research methods. Multiple authorships were shown to be an important determinant of the impact of the research being produced and its likelihood of being cited.¹⁷ The complexity and cost of medical research today requires multiple levels of expertise in various disciplines as well as accountability and oversight by study team members, institutions, and funding bodies. It is known that the number of authors per article has increased over the past few decades^18,19 with a concern posed to question the roles of multiple authors and the most senior academics holding senior authorship at the expense of others in the team.²⁰ Other studies have reported that the research produced by teams rather than single authors was impactful and more frequently cited, at least in certain fields.²¹ It is likely that multiple authorships arising from collaborative efforts have advantages of producing good quality impactful research; however, multiple authorships also have limitations and may not be feasible at every setting due to geographical limitations or strict timeline to follow as bringing more authors is time-consuming.²² In this review, we found that having multiple authorships is important to have publications with better adherence to reporting guidelines. However, the role of each author and the hierarchy of authorship should be clarified for successful collaborations and research impact as discussed earlier.

Study factors that improved adherence to reporting guidelines included well-designed, detailed study methods and adequately powered studies. Study results could be altered regarding trial designs, qualities, and methods.²³ Therefore, guidelines such as CONSORT statement that is designed for randomized control trials (RCTs), STROBE guideline for observational studies, and PRISMA guideline for systematic reviews were invented accordingly based on different study designs. RCTs are also considered as the highest level of primary evidence in the clinical practice, and therefore it is vital that these trials are reported according to the expected standards.²⁴

Other factors reported that might improve the level of adherence to reporting guidelines included journals endorsing these guidelines. The Internal Committee of Medical Journal Editors (ICMJEs) recognized the importance of reporting guidelines in ensuring study details that are described adequately to be evaluated appropriately and encouraged journals to request these reporting standards from authors.²⁵ The EQUATOR Network has valuable resources and tool kits to assist authors and journal editors to adopt the reporting guidelines and provide case studies of journals endorsing the guidelines. Since journals that endorsed reporting guidelines often ask authors to submit a completed checklist regarding the guidelines, it improves the quality of reporting for those journals endorsing these guidelines. Yet, not all journals currently endorse the guidelines. According to the CONSORT website, there are 585 journals that endorse CONSORT,²⁶ while there are about 30,000 journals indexed in PubMed.²⁷ While not all of these indexed journals publish RCTs, many of them do publish them, but do not adhere to CONSORT guidelines.²⁷

The EQUATOR Network also has tool kits for ethics boards and study sponsors to ensure that the reporting guidelines are considered when these agencies review research submissions for ethical approval or funding requests. It is therefore important that all stakeholders take part in the use and dissemination of the reporting guidelines to enhance the quality of medical research and biomedical literature.

Limitations

The included studies are limited to only eight of the reporting guidelines, and therefore the current study lacks the generalizability to other guidelines that may have a better adherence standard. In addition, there was no comparison between studies to ensure that they are using qualitative descriptors such as “inadequate” or “suboptimal” with the same operational definition. The studies do not provide sufficient information regarding the operationalization of qualitative descriptors to allow us to adequately compare descriptors across studies.

In addition, the study was limited to systematic reviews that present with its own set of limitations. The most notable limitation is the low mean score on the quality assessment since each systematic review follows different reporting guidelines or does not follow guidelines at all and the lack of detailed data on the included studies’ characteristics. Furthermore, a quantitative analysis was not conducted, as not all included studies provided relevant data. Strict inclusion criteria may have allowed a quantitative analysis. However, for the sake of a more representative sample, such criteria were not implemented.

The inclusion of studies in English only is also a limitation to a selected section of the medical literature and did not include other reporting guidelines that may be in use in other languages.

Despite the limited scope of inclusion criteria and quality limitation of the included studies, this review provides an insight into the limited uptake of reporting guidelines and calls for exploring barriers to such uptake. Future studies may include broad surveys of authors, journal editors, funding agencies, ethics boards, and readers to solicit opinions and understanding of the role of reporting guidelines in the medical research and literature.

Conclusion

Current adherence to reporting guidelines in the medical literature is suboptimal. However, there are factors associated with better reporting upon which we can develop strategies for better reporting. Reporting guidelines are an imperative tool in the endeavor to improve the consistency of reporting in the medical literature. However, the suboptimal uptake and correct usage of reporting guidelines demonstrate the need for further emphasis in the scientific community to encourage the use of reporting guidelines. The responsibility for improving the transparency, quality, and reproducibility of medical literature lies with all stakeholders from the research participants to regulatory authorities and everyone in between including authors, readers, educators, funders, academic and health care institutions, editors, peer reviewers, and guideline developers. Future studies may include broad surveys of authors, journal editors, funding agencies, ethics boards, and readers to solicit opinions and understanding of the role of reporting guidelines in the medical research and literature.

Data sharing statement

Unpublished study data are available upon request.

Author contributions

Contributed to the conception and design of the study, development of data extraction forms, search strategy, analysis of results, manuscript writing, and final review of the manuscript: YJ, NS, IS, CL, HS, and GL. Contributed to the methodological design, critical revision, and final review of the manuscript: MB, LZ, BB, MW, LPFA, IN, AL, LM, MM, YC, GS, MAHL, JDA, and LT. Substantially contributed to the conception and design of the study, critical revision, and final approval of the manuscript: ZS. All the authors read and approved the final manuscript. All the authors consented and approved the manuscript for publication. All authors contributed toward data analysis, drafting and revising the paper and agree to be accountable for all aspects of the work.

Disclosure

The authors report no conflicts of interest in this work.

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