ORIGINAL ARTICLE: INFERTILITY

Quality of reporting in infertility journals Demian Glujovsky, M.D., M.Sc.,a,b Carolina Boggino, M.D.,b Barbara Riestra, M.D.,b Andrea Coscia, M.D.,b Carlos E. Sueldo, M.D.,b,c and Agustín Ciapponi, M.D., M.Sc.a a Cochrane South-American Branch, Institute for Clinical Effectiveness and Health Policy (IECS), and b Center for Studies in Genetics and Reproduction (CEGYR), Buenos Aires, Argentina; and c Department of Obstetrics and Gynecology, University of California San Francisco, San Francisco, California

Objective: To evaluate whether fertility and top gynecology journals indexed in PubMed require the use of reporting guidelines and to identify the percentage of randomized controlled trials (RCTs) published in 2013 that were written following CONSORT guidelines in the top four fertility journals (by their highest impact factor). Design: Cross-sectional study evaluating instructions for authors and RCTs published in fertility journals. Setting: Academic institution. Patient(s): None. Intervention(s): None. Main Outcome Measure(s): Proportion of instruction-for-authors documents that suggested or required the use of reporting guidelines, and proportion of RCTs published in 2013 that accomplished the CONSORT checklist. Result(s): In 47% (16/34) of the journals one or more reporting guidelines were mentioned in the instructions for authors' documents. PRISMA and CONSORT were the most commonly mentioned reporting guidelines. None of the analyzed RCTs completed the 25 items of CONSORT guideline. Sequence generation or allocation concealment was not described in 69% of the studies. One-third of the journals did not publish a flowchart, 72% did not show relative and absolute size-effect measures, and 42% did not use measures of imprecision. In the summaries, 42% did not discuss the limitations of the study and 78% did not mention the generalizability of the results. Conclusion(s): Less than half of the analyzed peer-reviewed journals request the authors to use reporting guidelines. Nevertheless, among the top fertility and gynecology journals, reporting guidelines are widely mentioned. Overall, accomplishment of CONSORT items was suboptimal. Editorial boards, reviewers, and authors should join efforts to improve the quality of reporting. (Fertil SterilÒ 2014;-:-–-. Ó2014 by American Society for Use your smartphone Reproductive Medicine.) to scan this QR code Key Words: Reporting quality, reporting guidelines, fertility journals, randomized controlled and connect to the trials Discuss: You can discuss this article with its authors and with other ASRM members at http:// fertstertforum.com/glujovskyd-quality-reporting-infertility-journals/

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ransparent and accurate reporting of research studies is crucial to enhance reliability and value of medical research (1). Reporting means to relate, tell, present, or describe the findings of the study. It is not only important to perform a study, with an appropriate design and analysis, but it is also important to convey to the readers that the authors followed accepted reporting guidelines in

writing their articles. Studies should be properly described, so the readers may fully understand and interpret the results reported, as well as evaluate the internal and external validity. There is a responsibility involved in publishing a study, shared by the authors, the editorial board, and reviewers. When a published article is not fully or properly described, risk of misinterpretation may have a negative impact in clinical

Received August 6, 2014; revised October 13, 2014; accepted October 15, 2014. D.G. has nothing to disclose. C.B. has nothing to disclose. B.R. has nothing to disclose. A. Coscia has nothing to disclose. C.E.S. has nothing to disclose. A. Ciapponi has nothing to disclose. Reprint requests: Demian Glujovsky, M.D., M.Sc., CEGyR, Reproductive medicine, Viamonte 1432, Buenos Aires (C1055ABB), Argentina (E-mail: [email protected]). Fertility and Sterility® Vol. -, No. -, - 2014 0015-0282/$36.00 Copyright ©2014 American Society for Reproductive Medicine, Published by Elsevier Inc. http://dx.doi.org/10.1016/j.fertnstert.2014.10.024 VOL. - NO. - / - 2014

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practice or future research (2). Furthermore, readers may disregard valuable research exclusively due to reporting problems. Reporting guidelines are useful tools to write an article or when reporting a study. Reporting guidelines are geared toward reducing reporting bias and to describe step by step, how the research was performed. It also helps readers to judge the reliability of a study. These guidelines usually have checklists, flow diagrams, and texts that provide advice on how to report research studies (3). It is important to report consistently methods and findings of the research performed, and these guidelines provide an order, a format, and also show examples on 1

ORIGINAL ARTICLE: INFERTILITY how it was done. Some studies have evaluated the impact of using reporting guidelines and showed that the implementation of these guidelines increased the frequency of completely reported trials (4, 5). Reporting guidelines are free and fully available through initiatives such as Equator (Enhancing QUAlity and Transparency Of health Research), a network that gathers and promotes most of those guidelines (6). Some of the most commonly used guidelines are: CONSORT, TREND, STARD, STROBE, PRISMA, COREQ, SQUIRE, REMARK, ENTREQ, and CHEERS (7–16). Reporting guidelines should not only be used by authors, but should also be encouraged by editorial boards to enhance the quality of their own journals. Promoting the use of reporting guidelines could be encouraged under different strategies: [1] including them in the journal's instructions to authors (as suggested or required); [2] providing the authors with the checklist as a necessary step; and [3] encouraging the journal reviewers to use these guidelines to assess the evaluated studies before accepting them for publication (17). At present, more than 1,300 journals follow the Recommendations for the Conduct, Reporting, Editing and Publication of Scholarly Work in Medical Journals of the International Committee of Medical Journal Editors (18). This organization suggests using reporting guidelines while preparing a manuscript for submission, and encourages journals to request authors to follow these guidelines. Fertility journals are working diligently to improve the quality of the material accepted for publication. Recently, the leading fertility journals have published most randomized controlled trials (RCTs) with low risk of bias showing that authors and editors give relevance to methodological quality (19). However, the proportion of good quality designs was low, and that there is a need to keep working on improving the quality of publications in fertility journals. In 2006, Dias et al. (20) published a study that evaluated CONSORT in RCTs, and in 2009, Partsinevelou and Zintzaras (21) reported on quality of publications in polycystic ovary syndrome (PCOS). Despite these isolated efforts, a focused reporting quality evaluation among fertility journals is still missing. Our primary objective was to assess whether the journals indexed in PubMed that publish fertility articles, suggest or require the use of reporting guidelines and how this is done. A second objective was to assess whether CONSORT guidelines were followed in the published RCTs, in 2013, among the leading four fertility journals and the major three gynecology journals, which may also publish fertility articles.

MATERIALS AND METHODS This is a cross-sectional study and the specific STROBE statement was followed (10). During January 2014, we accessed the instructions-for-authors documents that were available at each website of all the journals that are indexed in PubMed, whose main topic was reproductive medicine or infertility. If more than one journal referred to the same instructions-forauthors document, it was analyzed only once. To locate those journals, we performed a search in PubMed using the 2

following strategy: reproduct* OR fertility OR infertility (filters: currently indexed in MEDLINE). In addition, we searched in the three gynecology journals (British Journal of Obstetrics and Gynaecology, American Journal of Obstetrics and Gynecology, and Obstetrics and Gynecology) with the highest impact factor, which may also publish fertility articles (22). In each online instructions-for-authors document, we evaluated whether Equator Network and/or International Committee of Medical Journal Editors were mentioned, whether any registration for RCTs was required, and whether any of the following reporting guidelines were specifically required or suggested: CONSORT, PRISMA, and STROBE. To decrease the risk of bias, this part of the study was performed first by three investigators (A.C., C.B., and B.R.) and then evaluated by another investigator (D.G.). After we performed a subgroup analysis. As was done in a previous publication (19), we selected the four fertility journals with the highest impact factor (IF), according to the 2013 impact factor (from the Institute for Scientific Information) and the H index (from SciMagO). The impact factor reflects the average number of citations of recent articles published in a particular journal, and could be used to estimate the importance of that journal (23, 24). We analyzed the top four fertility journals that usually publish clinical studies, and we added the evaluation of the three gynecology journals mentioned previously. In addition to the evaluation of the instructions-for-authors documents, on May 14, 2014, we performed a search in PubMed, identifying the potential RCTs (limits, type of article: RCT) published in 2013 by those journals, to analyze whether they followed each of the recommendations of the CONSORT guidelines. To determine the level of adherence to each item of the CONSORT, the most popular guideline, we identified all the actual RCTs whose main topic was infertility or reproductive medicine, analyzing each potential retrieved RCT by pairs of independent reviewers, evaluating the titles and abstracts of identified articles, according to prespecified criteria, using EROS software (25). As a second step, two reviewers (D.G., B.R., A.Co., C.B., and A.Ci.) randomly selected, extracted, and independently assessed each included study using the CONSORT checklist, analyzing how each RCT was reported. Discrepancies were resolved by consensus. We used proportion and 95% confidence interval to describe each of the evaluated parameters. To test differences between proportions we used the c2 test with Fisher's exact test. For statistical analysis we used software STATA 11.2.

RESULTS We found online instructions-for-authors documents in 34 of the 38 analyzed journals that publish fertility articles and were indexed in PubMed in January 2014. In 47% (16/34) of the journals, one or more reporting guidelines were mentioned in at least part of the author's instructions. Considering all seven journals with high IF, all of them mentioned reporting guidelines. PRISMA (7 of 7) and CONSORT (6 of 7) were the most commonly mentioned reporting guidelines. In these journals, EQUATOR is specifically cited in Human Reproduction and Reproductive Biomedicine Online VOL. - NO. - / - 2014

Fertility and Sterility® (RBM), British Journal of Obstetrics and Gynaecology, and Obstetrics and Gynecology, and also International Committee of Medical Journal Editors recommendations with its website link is present in all of them (Table 1). To analyze whether RCTs followed CONSORT guidelines, we evaluated 61 articles by title and abstract, and included 40 articles to be assessed by full text. We found that 36 of the 40 potential RCTs were indeed real RCTs, whose main topic was infertility or reproductive medicine, and were published in Fertility and Sterility (FS), Human Reproduction (HR), or RBM. We had neither exclusions nor missing data. None of the analyzed articles accomplished the 25 items of the CONSORT guideline. Of those 36 articles (21 from FS, 8 from HR, and 7 from RBM), only 25 (69.4%) identified the study as a randomized trial in the title. The introduction in those articles did not include a clearly identified objective in 25% of the cases. In the Materials and Methods section, the most common flaws were that trial design (including allocation ratio) was not stated in 30%, setting and location was not detailed in 30%, prespecified outcome measures were not completely defined in 28%, and no information about how sample size was determined in 28%. Regarding the randomization, 22% did not specify the method for the sequence generation, 58% did not mention the method for allocation concealment, 64% did not explain who implemented each procedure, and 42% did not report whether it was a blind study. In the Results section, the flowchart was not available in 36%, losses and exclusions were not reported in 33%, and dates of recruitment were not included in 56% of the articles. In the same section, effect size and its precision were not found in 42%, the relative and absolute effect size were not present in 72%, and harms were not reported in 58%. In relation to the Discussion section, 58% did not mention any limitation of the study and 78% failed to report the generalizability, which by the way was the least accomplished item. Finally, 36% did not mention whether the study had a registration number in any trial database, 69% did not report where to find the protocol of the study, and 31% did not report whether there was any funding for the study (Fig. 1).

We also found relevant associations between some usual failures and the journal where the studies were published, which are related to the editorial of those journals and the structure of those publications. Specifically, the structured abstract suggested by CONSORT guidelines were routinely used in FS and HR, but not in the seven articles analyzed from RBM. Also funding was not reported in five of the seven (71%) articles in RBM, whereas this failure occurred in less than 24% in FS and HR (P¼ .04 compared with RBM). Although some other trends were noticed, our sample size was too small to find more statistically significant associations.

DISCUSSION Our study found that some peer-reviewed fertility journals do not suggest or request the authors to use reporting guidelines. Nevertheless, in the seven commonly cited fertility and gynecology journals, reporting guidelines are widely mentioned. This is especially true for CONSORT and PRISMA, which are the reporting guidelines for RCTs and systematic reviews, respectively. Yet some other study designs that are frequently used, such as STROBE for observational designs and STARD for diagnostic accuracy, should also be present in any author's guideline. This part of our study has the limitation that we could only evaluate online author instructions. During the process of submitting a manuscript, some journals provide the authors with suggestions and recommendations, and those were not evaluated in the present article. Another limitation is that, despite reading the instructions-for-authors documents as pairs of independent reviewers, we could have involuntarily skipped over some instructions. Nevertheless, the use of an independent pair of reviewers, as it is done in systematic reviews, should have reduced this error risk. A third limitation is that we analyzed only journals published in PubMed and, therefore, we cannot extend these results to all fertility journals. A fourth limitation is that the confidence intervals in our data were wide, suggesting low precision. However, the upper

TABLE 1 Reporting guidelines in the most commonly cited journals that publish about infertility: instructions-for-authors documents. Journal

Strength of How it is Strength of How it is CONSORT recommendations recommended PRISMA recommendations recommended

FS HR HR Update RBM

Yes Yes No Yes

Should Must

Checklist Checklist Checklist

Yes Yes Yes Yes

Should Must Must Should

Must

BJOG

Yes

Must

Checklist

Yes

Must

AJOG

Yes

Must

Yes

Must

Yes

Must

Link to the guideline Checklist

Obstetrics & Gynecology

Yes

Must

Checklist Checklist Checklist Mention the guideline Checklist

Link to the guideline Checklist

Other guidelines STROBE, STARD, STREGA No Quadas Moose STROBE, MOOSE, STARD, STREGA, TREND, COREQ, SQUIRE, REMARK, ORION, STRICTA, REDHOT, CHEERS STROBE, MOOSE, STARD STROBE, MOOSE, STARD

AJOG ¼ American Journal of Obstetrics and Gynecology; BJOG ¼ British Journal of Obstetrics and Gynaecology; FS ¼ Fertility and Sterility; HR ¼ Human Reproduction; HR Update ¼ Human Reproduction Update; RBM ¼ Reproductive BioMedicine Online. Glujovsky. Reporting quality in infertility journals. Fertil Steril 2014.

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ORIGINAL ARTICLE: INFERTILITY

FIGURE 1

CONSORT checklist accomplishment in randomized controlled trials of the most commonly cited journals that publish about infertility. 95% confidence interval is showed between parentheses. The following items could be analyzed in some studies and were not included in this figure: 3b-Changes to methods; 6b-Changes to outcomes; 7b-Interim analysis; 11b-Similarity of interventions; 12-b Subgroup analysis; 14bTrial end or stop; 18-Ancillary analysis. Glujovsky. Reporting quality in infertility journals. Fertil Steril 2014.

limit of the interval is still high, therefore it may be concluded that many CONSORT items were not correctly accomplished. In the second part of our study, we saw some flaws that reduced the quality of the reports (Table 2). Less than 70% of the RCTs had a title mentioning the study design; however, this is very easy to improve, requiring the addition of this concept to the instructions-for-authors documents. Also, as readers often decide which article to read by looking at the abstract, presenting a useful abstract is critical. Both in FS and in HR the abstract is structured, including the items recommended by CONSORT. However, RBM does not have a structured abstract, therefore most of the RCTs published in this journal do not meet this recommendation. (This could also be easily improved by the editorial board.) In the Introduction section, a common problem is that often authors do not describe correctly the objectives of the study. To understand the objectives, authors could use the components of the PICO question, where population/persons/patients, intervention, comparison, and outcomes are mentioned (26). Although CONSORT does not state how objectives should be written, it does recommend being specific on this point. In the Materials and Methods section, almost one-third of the articles failed to mention the setting and location, and this was more commonly seen in multicenter studies. In some of the articles, the intervention was not well described because the authors state that it was described elsewhere, listing the reference. This is not ideal, as many readers do not have access to the source where the intervention was explained, therefore a brief description should also be included. More than two-thirds of studies analyzed were limited by the lack 4

of description of the sequence generation or the allocation concealment, which are two different items. If they are not identified by the author, one of them will be missed and the reader will not know who carried out each of these steps. This is crucial, because quality criteria include these two items (27). Another flaw frequently encountered is that some authors failed to explain the allocation ratio, especially when it was 1:1. In the Results section, the flowchart is a very useful tool for the reader, but it was absent in more than 30% of cases. This figure could be proposed by the editorial boards as being mandatory, in an attempt to improve the reader's understanding. Losses and exclusions are usually missing, if a flowchart is not present. Authors should be encouraged to include these data. Estimated effect size and precision are essentials to understanding the impact of the intervention, but in more than 40% of cases, just a P value or a summary value without a confidence interval is present (28). Although the relative effect size was commonly seen, the absolute effect sizes with its confidence interval was present in less than 25% of the studies, and this could lead the reader to draw incorrect conclusions (27). In addition it would be very informative to include the minimal clinically important difference (also known as MCID), defined as the smallest change in treatment outcome that a patient would identify as important (29). In the Discussion section, a high proportion of studies failed to mention the limitations of the study and the generalizability of the results. Also of significance, there are authors who placed information in the abstract, but then the same data was missing in VOL. - NO. - / - 2014

Fertility and Sterility®

TABLE 2 Improving study reporting: flaws commonly encountered and suggestions for improvement. Flaws

Suggestions

Abstract

Abstract

 Data are present in the abstract but not in the full text

 Check that all the data in the abstract are also present in the full text

Introduction

Introduction

 Incomplete objective(s) description

 Use PICO question components

Materials and Methods

Materials and Methods

 Setting and location poorly described  Intervention(s) not clearly described  Sequence generation and/or allocation concealment not reported

 Check this item especially in multicenter studies  Avoid citing a reference or at least include a brief description that clearly reproduces the intervention  These two items are different, describe both of them

Results

Results

 Flowchart is missing  Effect size and a precision measure are missing  Absolute effects measures are missing

 A flowchart helps the readers better understand the design  Use, for example, relative risk, odds ratio, mean, median, and confidence intervals  Include ARR, NNT, or any other absolute measures, as well as the minimal clinically important difference

Discussion

Discussion

 Limitations of the study are not described  Generalizability is not discussed

 Explain why the reader should be cautious about the results reported due to the limitations of the study  Mention whether extrapolation of the data is possible

Note: ARR ¼ absolute risk reduction; NNT ¼ number needed to treat; PICO question ¼ population/patient; intervention; comparator; outcome. Glujovsky. Reporting quality in infertility journals. Fertil Steril 2014.

the full text. It is advisable that abstracts be summaries of the full text. It means that abstracts should not add new information, but summarize the already existing data. Another problem often encountered is that some authors only mentioned funding if they received any, but they fail to include a statement when no funding was received, perhaps assuming that a statement of nothing to disclose is sufficient. Last, there were authors who placed information in the inappropriate sections, although the data were accurate. Whereas this is better that than not including the data, it could be easily improved if CONSORT recommendations are followed. Because there were inconsistencies found in trials reporting on infertility treatments, the consensus IMPRINT was recently published. Modifications to CONSORT were introduced, addressing the unique aspects of infertility treatments

TABLE 3 Items that publication authorities may consider to improve study reporting. Require authors to use structured abstracts. Include a list of available reporting guidelines with a link. Require the use of reporting guidelines. Include in the submission process a declaration that the study meets all the reporting guidelines and an explanation if exempted. Consider that peer reviewers check the use of reporting guidelines. Promote EQUATOR guidelines and ICMJE recommendations. Glujovsky. Reporting quality in infertility journals. Fertil Steril 2014.

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(30, 31). The consensus main focus were on reporting live birth rates as primary outcome, and that harms during the pregnancy and neonatal period be systematically included and reported, with the ultimate goal of increasing the transparency of benefits and risks of infertility treatments. The EQUATOR network promotes transparent and accurate reporting of research studies, and offers a free website for any author interested in using this type of guidelines. Some journals not only recommend or require the use of some reporting guidelines, but specifically cite EQUATOR with a link to its website. The more structured a research study is, the lesser the chance for error and the higher the likelihood to be understood by readers. Good reporting is the responsibility of each part involved in a path to a publication (Table 3). Editorial boards should encourage authors to use the reporting guidelines, ideally as mandatory requirements, and reviewers should check its use. Because editorial boards are ultimately responsible for the publications, they should implement all the available tools to improve the quality of the reporting. When journals provide links to the reporting guidelines, or to the guideline and the checklist, authors would be more likely to use them, in comparison with when the guidelines are just mentioned in the instructions-forauthors documents. Another option is to give authors a flexible template to help them meet the minimal reporting requirements. Authors' responsibility does not end by using a correct study design, but they also need to report their results accurately and in a methodical manner. Research studies that are not well reported could be misunderstood, 5

ORIGINAL ARTICLE: INFERTILITY and communicating results properly is a moral imperative for researchers. In conclusion, editorial boards, reviewers, and authors should join efforts to improve the quality of reporting in reproductive medicine. Acknowledgment: The authors thank our librarian Daniel Comande for his work in the search strategy.

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