Antequera et al. Systematic Reviews (2022) 11:281 https://doi.org/10.1186/s13643-021-01867-3 RESEARCH Open Access Lack of sex-related analysis and reporting in Cochrane Reviews: a cross-sectional study Alba Antequera1*† , M. Ana Cuadrado‑Conde2†, Emilia Roy‑Vallejo3†, María Montoya‑Martínez4†, Montserrat León‑García1†, Olaya Madrid‑Pascual5†, Sara Calderón‑Larrañaga6† and on behalf of Research for gender equity collaboration Abstract Background: Sex-specific analysis and reporting may allow a better understanding of intervention effects and can support the decision-making process. Well-conducted systematic reviews (SRs), like those carried out by the Cochrane Collaboration, provide clinical responses transparently and stress gaps of knowledge. This study aimed to describe the extent to which sex is analysed and reported in a cross-section of Cochrane SRs of interventions, and assess the association with the gender of main authorships. Methods: We searched SRs published during 2018 within the Cochrane Database of Systematic Reviews. An inves‑ tigator appraised the sex-related analysis and reporting across sections of SRs and collected data on gender and country of affiliation of the review first and last authors, and a second checked for accuracy. We conducted descriptive statistics and bivariate logistic regression to explore the association between the gender of the authors and sex- related analysis and reporting. Results: Six hundred and ten Cochrane SRs were identified. After removing those that met no eligibility criteria, 516 reviews of interventions were included. Fifty-six reviews included sex-related reporting in the abstract, 90 considered sex in their design, 380 provided sex-disaggregated descriptive data, 142 reported main outcomes or performed subgroup analyses by sex, and 76 discussed the potential impact of sex or the lack of such on the interpretations of findings. Women represented 53.1 and 42.2% of first and last authorships, respectively. Women authors (in first and last position) had a higher possibility to report sex in at least one of the review sections (OR 2.05; CI 95% 1.12–3.75, P=0.020) than having none. Conclusions: Sex consideration amongst Cochrane SRs was frequently missing. Structured guidance to sex-related analysis and reporting is needed to enhance the external validity of findings. Likewise, including gender diversity within the research workforce and relevant authorship positions may foster equity in the evidence generated. Keywords: Gender bias, Systematic reviews, Equity, External validity, Reporting Background Since the beginning of medicine and across disciplines, † Alba Antequera, M. Ana Cuadrado-Conde, Emilia Roy-Vallejo, María Montoya- white males have been considered the biological standard Martínez, Montserrat León-García, Olaya Madrid-Pascual and Sara Calderón- for all health conditions, and research on nonreproduc- Larrañaga contributed equally to this work. tive health of the female population has been tradition- *Correspondence: alba.antequera.martin@gmail.com ally ignored [1, 2]. Female participants have, by extension, 1 Biomedical Research Institute Sant Pau, Hospital de la Santa Creu i Sant Pau, been underrepresented and overlooked not only in medi- Barcelona, Spain cal schools but also in basic and clinical research [3–7]. Full list of author information is available at the end of the article © The Author(s) 2021. 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The Creative Commons Public Domain Dedication waiver (http://​creat​iveco​ mmons.​org/​publi​cdoma​in/​zero/1.​0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Antequera et al. Systematic Reviews (2022) 11:281 Page 2 of 8 For example, in the USA after institutional efforts of the numbers at manageable levels for fast human screening National Institutes of Health (NIH) over the last several and data extraction. decades [8, 9], the percentage of females included in clinical trials funded by the NIH reached up to 50% [10]. Identification of Cochrane reviews and data extraction Nevertheless, an increase of female representation in We searched for Cochrane reviews using the advanced study samples has not led to an improvement in the anal- search option within the Cochrane Database of Sys- ysis and data disaggregation by sex or gender [11, 12], i.e., tematic Reviews from January 1, 2018, to December 31, ‘gender bias’ [13], and it may carry avoidable risks, espe- 2018. Two authors (from AA, ACC, ERV, MLG, SCL) cially for the underrepresented population. For example, independently screened titles and abstracts, and when sex/gender analyses may guide specific recommendations appropriate, full-texts. We developed and pre-tested a based on differential effects for sexes, as tailored drug data extraction form in Excel to collect data on gender doses or relation benefits-harms of certain procedures and country affiliation of first and last review author, [14, 15]. and sex- and gender-related analysis and reporting in Sex and gender are interrelated concepts but not syn- SRs (i.e., review authors used any sex or gender-related onyms. Sex refers to biological traits, whereas gender is terms to provide information across the SR). One author based on socially constructed features [16]. Although (from AA, ACC, ERV, MLG, SCL) extracted data on genetic, cellular, biochemical, and physiological differ- sex-related reporting in the following review sections: ences between males and females have been described abstract, methods, results, and discussion. This manual for decades [17, 18], and several initiatives from grant inspection also involved the Control-F search command agencies and journals and editors are underway to tackle to look for keywords such as “male”, “female”, “women”, the scarce attention to sex and gender in biomedical sci- “men”, “woman”, “man”, “sex” and “gender”. A second ence [19–22], there remains a lack of sex and gender inte- author (from AA, ACC, ERV, MLG, OMP, SCL) checked gration in evidence production, both in primary studies data extraction for accuracy verification. For the results and systematic reviews (SRs) [23, 24]. section, we made the difference between a descriptive The Cochrane Library is a collection of databases that assessment, as sex-disaggregated data reported either contain high-quality, independent SRs to inform clinical in the main text or table of characteristics of included practice and health policy. The Cochrane Equity Methods studies, and analytic approaches, as sex-disaggregated Group recently developed a tool to help review authors to results from pooling data from primary studies through improve sex and gender reporting in their SRs [25]. How- the main meta-analysis or subgroups analyses. We rated ever, Cochrane SRs might not be exempt from gender as non-applicable in the results and discussion sections bias [26]. Meanwhile, a recent study suggested that the assessment, those reviews that reported no studies meet- presence of women in main authorship positions might ing the eligibility criteria or included insufficient studies improve the degree of sex and gender consideration in to perform pre-specified analyses. We determined the research [27]. Biological and social-based differences gender of the first and last review authors by name when lead to differential health risks, disease incidence, and provided a reasonable reliance on the perceived gender of health service needs [28]. Thus, a systematic assessment the investigators; otherwise, we used Gender-API soft- of sex-related reporting and analysis may support differ- ware [29]. In the case of names that might be assigned ent approaches of intervention for specific patient groups for both genders or assignation remained doubtful, we (especially, when the benefit-harm balance remains grouped the given name, family name, and affiliation unclear for certain interventions) and highlight gaps of institution details and tracked it on the institution web- knowledge for further more inclusive medical research. site and social media. In this paper, we accepted the We described the extent to which sex is analysed and sex and gender terminology used by the review author reported in Cochrane SRs of interventions published in regardless of the appropriateness of the terms [30, 31]. 2018, and assessed the relationship between sex-related Thus, hereafter, we used the “sex/gender” to mean sex analysis and reporting and gender of main authorships. and/or gender” terms for participants in reviews and the “gender” term for authors. Methods Eligibility criteria Data analysis We included Cochrane reviews on intervention studies. We described the frequencies for sex/gender reporting We excluded reviews that involved single-sex because in each of the aforementioned review sections, the gen- they addressed sex-specific health conditions, and those der of authorship in dominant positions, and author’s that had been withdrawn from publication. We restricted country of affiliation categorised according to the World the publication date to 2018 to remain the reference Bank country income index [32]. We dealt with missing Antequera et al. Systematic Reviews (2022) 11:281 Page 3 of 8 and non-applicable data by listwise deletion to calcu- Finally, we included 516 reviews of interventions in our late frequencies. We reported data as medians, percent- analyses. Figure 1 represents the PRISMA flow diagram. ages, and ranges. We performed different logistic models depending upon the review section to assess the odds of Characteristics of included Cochrane reviews sex/gender-related reporting. We did not use the income Two-thirds of included Cochrane reviews were updated index as a confounder to avoid ecological fallacy [33]. We versions. Four publications were individual publica- established statistical significance at P value of 0.05. We tion data systematic reviews [35–38]. Nine reviews were performed statistical analyses using STATA statistical signed by collaborative research groups, and seven of software (version 13; College Station, USA). them were conducted by the same group. The median number of authors was 5 (range 2–22). We identified Results 1,031 main authorship positions since one collaborative Selection of Cochrane reviews research group in one review was considered as a single We identified 610 Cochrane SRs with a publication date of signature. Women were first or last authors in 53.1% and 2018. We excluded 94 reviews from further analyses due 42.2% of the reviews, respectively. In 25.78% (133/516 to withdrawn publication (15 SRs), addressing sex-spe- SRs) of the cases, both authors were women, and in cific interventions (78 SRs), and testing the entomological 69.57% (359/516 SRs), at least one of the main authors effectiveness of long-lasting insecticidal nets (1 SR) [34]. was women. Although authors were widely distributed geographically, no authors were affiliated to institutions Fig. 1 Flow diagram showing the selection of systematic reviews Antequera et al. Systematic Reviews (2022) 11:281 Page 4 of 8 in low-income countries. Most authors (874; 84.7%) impact of sex (or the lack of such) on the clinical and came from high-income countries, over one-third of research implications. In addition, after pooling review them (378; 43.2%) based on the UK. sections, we found that 40.3% (208/516 SRs) of reviews reported on sex in at least two sections, and 2.7% (14/516 Sex/gender‑related analysis and reporting in Cochrane SRs) did it in all five sections. In the individual partici- reviews pant data (IPD) SR subset, we detailed that only one [35] Table 1 shows the overall sex/gender-related analysis out of the four IPD reviews reported both sex-disaggre- reporting in each of the sections assessed. Overall, 10.9% gated descriptive and analytic results and encouraged (56/516 SRs) of reviews included sex-related report- caution in the use of drugs assessed in the female group, ing in abstract sections, and 17.4% (90/516 SRs) consid- while the others only reported descriptive results by sex. ered sex in their methods. We judged 30 reviews to be We analysed distribution of frequencies between sex/ non-applicable for the results section assessment. Of the gender reporting and gender authorships as shown in remaining, 78.2% (380/486 SRs) of reviews presented Table 2. First woman authorship significantly improved sex-disaggregated descriptive data, while 31.9% (142/445 sex/gender reporting in the abstract section (P=0.019). SRs) amongst those that could pool data reported using SRs with woman in the last authorship positions an analytic approach by sex (i.e., main outcomes or per- showed a significant sex/reporting in descriptive results formed subgroup analyses by sex). As for the discussion (P=0.027). Amongst reviews in which both authors were section, we rated 16 reviews as non-applicable, whereas women, 39.3% and 35.5% of the SRs reported on sex/gen- 15.2% (76/500 SRs) of reviews reflected on the potential der in the abstract (P=0.015) and discussion (P=0.046), respectively. We carried out logistic regression to assess the pos- Table 1 Sex/gender-related analysis and reporting in Cochrane reviews sibility of reporting sex/gender depending on gender authorship (number of women authors in dominant posi- Review section Sex/gender Item was not tions) as shown in Table 3. SRs in which both authors reporting, % (N) applicable to SR, % (N) were women had a higher odd of sex/gender report- ing than SRs with none women authors in the following Abstract 10.9 (56) 0 comparisons: descriptive results section (OR 1.98, 95% Methods 17.4 (90) 0.2 (1) CI 1.11–3.55, P=0.021), and, after pooling any of the Descriptive results 78.2 (380)a 5.8 (30) assessed sections, in at least one section (OR 2.05, 95% Analytic results 31.9 (142)b 13.8 (71) CI 1.12–3.75, P=0.020), and three or more sections (OR Discussion 15.2 (76)c 3.3 (17) 1.97, 95% CI 1.07–3.62, P=0.030). For descriptive results At least two sections 40.3 (208) 0 having one woman as an author also increased the pos- At least three sections 16.3 (84) 0 sibility of sex/gender reporting (OR 1.65, 95% CI 1.09– All sections 2.7 (14) 0 2.70, P=0.046). Other comparisons found no significant Abbreviations: SR systematic review associations; however, they showed a positive and pro- a Denominator: Number of SRs that were applicable (N=486) gressive association for the number of women authors b Denominator: Number of SRs that were applicable (N=445) and sex reporting. c Denominator: Number of SRs that were applicable (N=500) Table 2 Sex/gender reporting by review section according to gender of authors Sex/gender reporting in each First author (female) Last author (female) Both authors f­ emalea At least one author review section female % (N) P value % (N) P value % (N) P value % (N) P value Abstract (N=56) 68% (38) 0.019 44.6% (25) 0.701 39.3% (22) 0.015 73.2% (41) 0.531 Methods (N=90) 55.6% (50) 0.623 50.0% (45) 0.105 28.8% (26) 0.465 76.7% (69) 0.114 Descriptive results (N=380) 56.1% (213) 0.147 45.0% (171) 0.027 28.1% (107) 0.127 72.9% (277) 0.012 Analytic results (N=142) 51.4% (73) 0.465 45.8% (65) 0.405 30.3% (43) 0.316 66.9% (95) 0.386 Discussion (N=76) 60.5% (46) 0.195 50.0% (38) 0.161 35.5% (27) 0.046 75.0% (57) 0.315 At least two sections (N=208) 56.7% (118) 0.175 45.2% (94) 0.266 29.3% (61) 0.130 72.6% (151) 0.221 At least three sections (N=84) 60.7% (51) 0.126 51.2%(43) 0.070 36.9% (31) 0.011 75.0% (63) 0.238 All sections (N=14) 57.1% (8) 0.759 57.1% (8) 0.253 35.7% (5) 0.389 78.6% (11) 0.459 a Both authors are women compared to at least one being a man Antequera et al. Systematic Reviews (2022) 11:281 Page 5 of 8 Table 3 Logistic regression sex/gender reporting by review for the analytic approaches (31.9%). Taken together, the section according to gender of authors repeatedly lower ratio of reporting on analytical items Review section OR CI 95% P value that we and others observed [24, 26] suggests a concern- ing lack of attention to the potential role of sex/gender Abstract in the study outcomes. In view with this, Morgan et al. One woman author 0.87 0.43–1.77 0.698 enhanced some considerations about the conception, Two women authors 1.88 0.67–1.87 0.079 development and data management which would foster Methods gender-related analysis in health system research [39]. One woman author 1.51 0.86– 2.66 0.154 The known insufficient data about sex/gender in primary Two women authors 1.56 0.83–2.93 0.164 studies [11, 12, 40] hinders its reporting in SRs. How- Descriptive results ever, when that is the case, the discussion section gives One woman author 1.65 1.09–2.70 * 0.046 authors the possibility to address such limitations. Still, Two women authors 1.98 1.11–3.55 * 0.021 we showed that only 15.2% of SRs addressed participants’ Analytical results sex/gender in their discussions. Clearly, when sex/gender One woman author 0.71 0.44–1.14 0.160 reporting is not considered a priority, the lack of the nec- Two women authors 1.03 0.62–1.73 0.904 essary data will likely be overlooked. Discussion This generalised lack of sex/gender consideration is One woman author 1.08 0.58–2.01 0.793 a matter of concern, which has led to the publication Two women authors 1.78 1.12–3.75 0.079 of relevant reporting guidelines and support tools by 1 or more sections internationally known research institutions, such as the One woman author 1.27 0.78– 2.05 0.333 Cochrane Collaboration, NIH or Canadian Institutes for Two women authors 2.05 1.12–3.75 * 0.020 Health Research [8, 16, 41]. However, despite policy and 2 or more sections institutional support, our results show that the problem One woman author 1.16 0.76–1.77 0.486 remains. Two women authors 1.49 0.93–2.38 0.099 We described a link between first and last women’s 3 or more sections authorship and the possibility of a sex/gender-related One woman author 1.07 0.59–1.93 0.827 analysis and reporting. Nielsen et al. provided strong Two women authors 1.97 1.07–3.62 * 0.030 evidence associating sex/gender-related analysis with All sections the presence of women in the author group, especially One woman author 1.4 0.34–5.68 0.638 in leading first and last author positions, using a sample Two women authors 2.00 0.47–8.55 0.347 of more than 1.5 million medical research papers [27]. A One woman: one woman in a main position authorship. Two women: two recent bibliometric analysis examining more than 11.5 women in a main position authorship million studies also showed an increased probability of Abbreviations: CI confidence interval, OR odds ratio reporting sex/gender in articles where the first and last authors were women [23]. Our findings, therefore, con- tribute to the existing debate on the relevance of women’s Discussion participation in science, as a means of counteracting and Our findings showed that overall sex/gender considera- even reversing institutional cultures that promote sex- tion in Cochrane reviews was inadequate, given that only blind research [1]. 2.7% of the SRs reported it in all five sections. When the In relation to the country of origin, no review was con- first and last authors were women, there was a higher ducted by authors affiliated to low-income countries. In possibility of sex/gender-related reporting. We also contrast, Sugimoto and colleagues found poorer rates of found a lack of representation of reviews produced in sex/gender-related reporting in North America, com- low-income countries. pared to under-resourced research settings, such as Our results are consistent with previous findings on Africa [23]. Larivière and colleagues found higher preva- insufficient sex/gender reporting in SRs [24, 31]. Interest- lence of women’s authorship in countries with lower sci- ingly, abstracts showed the lowest sex/gender reporting entific output, with South America and Eastern Europe of all sections (10.9%). This is both consistent with previ- being the regions with greatest gender parity [41]. In our ous work [26] and significant, especially considering that case, the scarcity of authors affiliated to low- and middle- abstracts are supposed to showcase the most relevant income countries has hampered the analysis of any rel- findings of a SR. Reporting in the methods section was evant variations. also inadequate (17.4%). Concerning the results sec- Our study has several caveats and limitations. First, we tion, we found that sex/gender reporting was highest in did not analyse whether sex/gender reporting was more the descriptive section (78.2%), and consistently lower Antequera et al. Systematic Reviews (2022) 11:281 Page 6 of 8 likely in disease-specific research areas as described of data and reinforcing regulation that ensures that the previously [40]. Second, external validity of SRs goes twin goals of diversity and excellence in science are met. beyond sex/gender and is influenced by other axes of inequity (and intersections between them) that have Abbreviations not been considered in this study [9, 42, 43]. Third, we CI: Confidence interval; NIH: National Institutes of Health; OR: Odds ratio; SR: acknowledge that our binary approach to sex and gender Systematic reviews. and the assignment of gender based on authors’ names Acknowledgements can be both problematic and inaccurate [44, 45]. Fur- The authors gratefully acknowledge ‘The Feminist Lancet’ initiative for inspir‑ ther, we used sex and gender terms interchangeably and ing this idea, María González-Barral for her input and support throughout the combined (‘sex/gender’) when referring to the degree of development of the study, and Meredith K. D. Hawking, Ana Dowrick, and Lucie Hogger for reviewing and commenting on the manuscript. Further‑ reporting in Cochrane SRs. However, we acknowledge more, the authors thank Maria Delius and Ralph Möhler for their insightful that sex and gender are different concepts [16]. Our comments to improve the clarity of this manuscript during the peer-review decision was pragmatic and shaped by the frequently process. inaccurate use of these terms in primary studies and Authors’ contributions Cochrane SRs. Finally, although we collected countries All authors contributed to the conception, design, analysis, and interpretation of affiliation, we used no this variable as a confounder of this study. All authors participated in the drafting of the manuscript and reviewed it. All authors approved the final version. in order to avoid the ecological fallacy [33]. Moreo- ver, we collected no additional variables that may have Funding been confounders, so we have not adjusted our mod- The authors have no funding sources to declare. The preliminary results were presented as Antequera A, León M, els. In terms of strengths, the number of SRs included Calderón S, Cuadrado A, Roy E. Sex and gender reporting and analy‑ in our study, as well as the peer reviewed rating system sis in Cochrane reviews: a cross-sectional methods study. Preliminary gave consistency to our research findings. To our knowl- results. [Abstract] BMJ Evidence-Based Medicine 2019,24(Suppl 1)A18- A19;doi:10.1136/bmjebm-2019-EBMLive.35. Evidence Live 2019, Oxford, edge, this is the first study investigating the association UK, July 15–17, 2019. between sex/gender reporting and gender of author- ship amongst Cochrane SRs. The fact that Cochrane SRs Availability of data and materials The data that support the findings of this study was derived from the fol‑ are used worldwide to support evidence-based clinical lowing resources available in the public domain: https://​www.​cochr​aneli​ practice and policy, make our findings of particular rele- brary.​com/​cdsr/​revie​ws. However, all the information is available from the vance, with the potential to inform high-quality research corresponding author upon reasonable request. Alba Antequera is a doctoral candidate in Public Health and Methodology of within Cochrane collaboration, and support rigorous Biomedical Research, at the Department of Pediatrics, Obstetrics, Gynaecology decision making worldwide. and Preventive Medicine at Universitat Autònoma de Barcelona (Spain) and Further Cochrane systematic reviews should enhance this work is part of her PhD. adherence to international reporting guidelines on sex and gender equity [30, 46]. The Cochrane Collabora- Declarations tion has developed structured guidance and tools tai- Ethics approval and consent to participate loring to sex- and gender-based analysis [24, 47], while Not applicable they may require amendments to be consistent with the Consent for publication current standards of conducting systematic reviews, Not applicable including health equity in the GRADE approach [48], when appropriate. Researchers, editors, and funding Competing interests The authors declare that they have no competing interests. organisations need to demand better sex- and gender- related analysis and reporting to achieve the purpose Author details 1 of conducting methodologically sound systematic Biomedical Research Institute Sant Pau, Hospital de la Santa Creu i Sant Pau, Barcelona, Spain. 2 Accident and Emergency Department, King’s College Hos‑ reviews. pital, London, UK. 3 Internal Medicine Department, Hospital Universitario de La Princesa, Madrid, Spain. 4 Servicio Murciano de Salud, Coordinación Estra‑ tégica para la Cronicidad Avanzada y Atención Sociosanitaria, Murcia, Spain. Conclusions 5 Arztpraxis Kalkbreite, Zürich, Switzerland. 6 Centre for Primary Care and Public Sex- and gender-blind research contributes to biased Health, Queen Mary University of London, London, UK. decisions in policymaking and health service provision. 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