Gender bias in biomedical research James S. Economou, MD, PhD, Los Angeles, CA

From the Department of Surgery, University of California, Los Angeles, CA

WOMEN HAVE BEEN ACHIEVING NEAR PARITY in MD and MD/PhD training, but their advancement in academic biomedical science is reduced at every career milestone thereafter. Women are significantly underrepresented even at the earliest points in the PhD pipeline, particularly in fields outside of biology. This is a troubling statistic that negatively impacts the talent pool and exacerbates career inequity in all areas of biomedical research. The major biomedical research themes that will command our attention in the 21st century---neuroscience, cardiovascular disease, oncology---will require large team science efforts integrating a diversity of scientific disciplines, including biology, engineering, sociology, chemistry, and medicine. These scientific teams must also integrate diversity in gender, race, and ethnicity to enrich and add value to their discoveries and to better serve a diverse and multicultural society. This editorial reviews factors that may actively impede women’s participation in biomedical research, at the level of graduate and postgraduate training, in their opportunities for career advancement in the professoriate, and in their competitiveness in securing research support. There are implicit biases---often subtle discrimination based on cultural stereotypes that may be outside of conscious awareness (unconscious bias)---that can affect decisions about one’s career at every level.1-3 Women might be viewed as having more communal and nurturing traits, whereas men might be expected to have more of a selfpromoting, leadership phenotype. Women seem to be conditioned from an early age to avoid violating their prescriptive gender stereotypes, or if they do so, risk being perceived as overly ambitious. Women also have a disproportionate Accepted for publication July 11, 2014. James S. Economou is Vice Chancellor for Research at UCLA and President-elect of the American Surgical Association. Reprint requests: James S. Economou, MD, PhD, 405 Hilgard Ave, 2147 Murphy Hall, Los Angeles, CA 90095. E-mail: [email protected] Surgery 2014;156:1061-5. 0039-6060/$ - see front matter Ó 2014 Elsevier Inc. All rights reserved.

responsibility for child care and family life, which is both a stereotype and a stressor in work-life balance. Unconscious biases likely have a pervasive impact on decisions at many levels with respect to recruitment, promotion, grant review, and even socialization in academic medicine. Perhaps the most important interventions in dealing with bias, how all of our brains attempt to organize and systematize our social lives, are to inform the academic community about its existence, its adverse impact, and to create greater objectivity and structure in evaluative processes. Various studies have shown that any reminder to women or minorities of their stereotyped identities can reduce their performance in that stereotyped task; this conscious or unconscious behavior is termed ‘‘stereotype threat.’’4 For example, female and male students performing a difficult math test in a threatening test environment---when informed that the examination is very difficult, that it is a measure of math aptitude, and that the results would be used to make gender comparisons---yielded poorer performance by women.5 Even simply informing the class that it was a difficult examination yielded similarly discordant scores. However, providing participants a brief description of stereotype threat and its effects in causing anxiety seemed to buffer its adverse effects and return women’s performance to equivalency with male students.5 A number of interventions may reduce stereotype threat in academic medicine.6,7 These include introduction of the concept in the academic community and promotion of an environment in which individuals are assured that their identities are strengths (identity safety). These stereotypes---which are laid out at a very young age---can incrementally disadvantage women in the field of biomedical research at every inflection point in their careers. The number of women enrolled in US medical schools has risen from 10% in 1970 to almost 50% today.8 But even as women have achieved parity in medical school classes, gender role stereotypes persist. Both women and men tend to view men as being more effective leaders,9,10 a gender role stereotype that is carried into professional schools and beyond. Wayne et al11 performed 2 studies to SURGERY 1061

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determine whether gender bias was occurring during the identification of discussion leaders in small group settings of medical students. Despite equivalency in gender representation, male medical students emerged as group leaders in a 2:1 ratio. In a subsequent study, instructions were given to the small groups that a leadership role was an important experience for everyone, a relatively nonspecific intervention that nevertheless resulted in leadership parity in this second cohort. MD/PhD programs are designed to produce highly trained physician-scientists who will engage in biomedical research. A somewhat lower proportion of women (40%) enter these combined programs, but women are overrepresented in noncompletion rates.12 This higher attrition rate has been attributed to work–family balance and the lack of women physician-scientist role models. Both of these factors contribute to the persistence of gender disparities in the biomedical research workforce. Despite equal numbers of women in medical school classes, parity with respect to rank attainment, salaries, and leadership has not been maintained as women enter the professoriate.13,14 Female representation in leadership positions--tenured professors, department chairs, institute directors, and deans---is in the 6–19% range.14 In 2011, 47% of medical school graduates were women, accounting for 37% of full-time faculty (44% of newly hired faculty), but only 13% at the rank of full professor (compared with 11% in 1980).15,16 This cannot be explained by lag-time bias because the upward trend in female representation in medical school graduation classes began 3 decades ago. Rather, there is a progressive stepwise attrition as women enter and progress through the professoriate. Jagsi et al17 conducted a nationwide survey of physician-scientists who received National Institutes of Health (NIH) K08 and K23 Career Development Awards in 2000–2003, using these as reasonable surrogates for beginning success in a research career. Male faculty had higher salary, even after adjustment for specialty, academic rank, leadership positions, publications, and research effort. Even women physician-scientists without children had lower incomes, which argues against a parental responsibility explanation. The actual shortfall in salary, which was about $12,000, is as important in financial terms as in its adverse impact on morale. Although the tenure system in medicine has remained intact, several alternative faculty tracks have emerged, the most predominant being that

Surgery November 2014 of the clinician-educator.16 This track, which emphasizes clinical practice and teaching, is populated by a greater proportion of women at a majority of academic medical centers; women often report teaching as the main reason for entering academic medicine.18 These nontenure tracks have less rigorous timetables for original scholarship and generally slower rates of promotion. The importance of physician-educators in academic medicine cannot be understated, but these career trajectories may be less conducive to a substantive career in biomedical research and may explain some of the differences noted. Although women enter the biomedical professoriate with objectively comparable levels of preparation for an academic career as men, there are various forms of bias, unconscious or otherwise, that likely cumulatively impact their socialization strategies in the academic workplace.19 Despite receiving poorer initial recruitment packages,20,21 such as financial support, space, and salary early in their careers, women investigators seem to have comparable success rates in F-, K-, and R-type awards.22 However, there is erosion in grant success rates in renewal applications, a trend for women scientists to submit fewer revised applications, and generally lower dollar grant budgets.2226 Parenthetically, Ginther et al27 reported that black investigators were 13% less likely to be awarded R01 grants even after controlling for educational background, training, and publications. These trends necessarily raise the question of unconscious bias in the review mechanism; however, the lack of a culturally supportive environment with role models and mentorship that promotes success may be a more likely explanation for this disparity. Whereas the MD pool is near parity and the MD/PhD cohort is improving, albeit with a higher attrition, the number of women in the PhD pipeline in STEM (Science, Technology, Engineering and Mathematics) is alarmingly low at the level of production (with the exception of life sciences), and in most fields is at single-digit percentages at the senior faculty ranks.28 In the life sciences, where the percentages of doctorates are essentially equivalent,29,30 this attrition as women enter the professoriate is also dramatic and may begin even at the level of their opportunities for postdoctoral training in leading laboratories led by prominent male scientists.31 The big research questions in biomedical research will require teams of scientists from diverse disciplines that must include chemistry, physical sciences, and engineering. Scientific solutions to these important questions will be

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shortchanged by the underrepresentation of both women and minority team members. There is also clear evidence of gender or sex bias even in the way research hypotheses are posed and tested.32,33 Large genomic analyses of murine somatic tissues show surprisingly widespread sexual dimorphism in thousands of differentially expressed genes.34 These differences are likely owing to the effects of testicular of ovarian hormones, but even relatively modest differences can contribute to gender phenotypes of complex diseases such as diabetes, atherosclerosis, and autoimmune disease. Yoon et al35 examined several thousand manuscripts from leading surgical journals and found that in 22% the sex of the experimental animals was not specified and, in those that did, 80% of studies included only male animals. This has led the NIH to issue policies to ensure that preclinical research balances sex in cell and animal studies.36 Even in the field of medical device approval, the enrollment of women in preapproval studies is not always consistent with gender preference of the disease.37 In the mid-1980s, the NIH established a policy for inclusion of women in clinical trials to allow for valid analyses, which was enacted into law in 1993 as the NIH Revitalization Act.38 Still, surveys have identified underrepresentation of women in some recent randomized trials.39 Our goal should be to create an academic climate conducive to gender equity in biomedical research.40 The culture of the work environment is probably the most important factor affecting women faculty experiences, and the academic climate will improve to the extent that the work environment can be constructed more effectively to support women’s careers, particularly at the level of assistant professors. Women may have greater challenges than men in integrating work and nonwork roles if they have a disproportionate share of nonwork responsibilities. It may require multilevel interventions to promote women’s career success and academic outcomes. A collegial environment will serve as an important determinant for women’s success in academia, a predictor of research productivity and career satisfaction, and an important element of women’s advancement and retention in the biomedical research workforce. Timely and constructive performance feedback on academic progress has also been shown to be strongly associated with career satisfaction.41 Programs that emphasize mentoring, career planning, and integration into networks of colleagues all contribute to faculty satisfaction, productivity, and retention.42,43 These goals are hindered by

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the scarcity of female role models and effective mentoring strategies. An academic culture should not penalize faculty for career interruptions or part-time service. A number of recommendations have been made along the lines of modifying the rigidity of the ‘‘tenure clock,’’ which creates considerable stress in women who may be building their families. Extension of the tenure period or part-time work strategies may help to address this. A number of programs have allowed for additional financial support for women transitioning back after family leave. Where these programs have been instituted, they seem to have changed the perceptions of junior women faculty with respect to the supportiveness of their environment (perhaps by increasing their confidence that they could succeed at their institutions because their institutions wanted them to succeed) and improved retention rates.21,44 Other recommendations include the provision of affordable onsite childcare or sick childcare, stressing the importance of gender equity in salary and institutional support for equivalently trained and promising faculty, and fostering a culture enhanced by strong mentors and role models as pathways toward developing an academic biomedical workforce with greater diversity. Finally, institutional policies that are transparent and accountable are central to overcoming bias. The leadership at the NIH has recognized the differences both in gender and racial disparities in receiving extramural grant support.22 The NIH has promoted Reentry45 and Diversity46 supplements, allows multiple principal investigators and parttime K Awards, and has extended leave policies on some of their other awards.47 The NIH also supports research to investigate the causal factors and interventions that support careers of women in biomedical science.48 Many of the recommendations of the NIH Working Group on Women in Biomedical Careers are being implemented.49 In summary, there will be substantial social, economic and scientific costs if we cannot improve the diversity of our biomedical research workforce. Although this essay has focused on gender disparity, the inequities and their adverse impact apply as well to racial and ethnic disparities in workforce representation. It should not be difficult for the readers of this leading surgical journal to appreciate these issues,14 to recognize how a scholarly discipline is greatly enriched by gender diversity, how significant progress can be made through constant attention by both institutions and professional societies, and how we still have significant shortfalls.

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The authors grateful for many discussions about gender bias with his colleagues: Professors Judith Gasson, Lynn Gordon, Vickie Mays, Vivian Pinn and Nancy Wayne. The author also thanks Jill Sweitzer, Amy Hawkins, and Jazmin Barajas for editorial comments. REFERENCES 1. Schiebinger L. Scientific research must take gender into account. Nature 2014;507:9. 2. Pololi LH, Civian JT, Brennan RT, Dottolo AL, Krupat E. Experiencing the culture of academic medicine: gender matters, a national study. J Gen Intern Med 2013;28:201-7. 3. Corrice AM. Unconscious bias in faculty and leadership recruitment: a literature review. Association of American Medical Colleges. Analysis in Brief 2009;9:2. 4. Spencer SJ, Steele CM, Quinn DM. Stereotype threat and women’s math performance. J Exp Soc Psychol 1998;35:4-28. 5. Johns M, Schmader T, Martens A. Knowing is half the battle: teaching stereotype threat as a means of improving women’s math performance. Psychol Sci 2005;16:175-9. 6. Thoman DB, Smith JL, Brown ER, Chase J, Lee JY. Beyond performance:a motivational experiences model of stereotype threat. Educ Psychol Rev 2013;25:211-43. 7. Burgess DJ, Joseph A, van Ryn M, Carnes M. Does stereotype threat affect women in academic medicine? Acad Med 2012;87:506-12. 8. Leadley J, Magrane D, Lang J, Pham T. Women in U.S. academic medicine: statistics and benchmarking report, 20072008. Washington, DC: American Association of Medical Colleges; 2008. 9. Rudman LA, Kilianski SE. Implicit and explicit attitudes toward female authority. Pers Soc Psychol Bull 2000;26:1315-28. 10. Heilman ME, Wallen AS, Fuchs D, Tamkins MM. Penalties for success: reactions to women who succeed at male gender-typed tasks. J Appl Psychol 2004;89:416-27. 11. Wayne NL, Vermillion M, Uijtdehaage S. Gender differences in leadership amongst first-year medical students in the small-group setting. Acad Med 2010;85:1276-81. 12. Andriole DA, Whelan AJ, Jeffe DB. Characteristics and career intentions of the emerging MD/PhD workforce. JAMA 2008;300:1165-73. 13. Martinez ED, Botos J, Dohoney KM, Geiman TM, Kolla SS, Olivera A, et al. Falling off the academic bandwagon. Women are more likely to quit at the postdoc to principal investigator transition. EMBO Rep 2007;8:977-81. 14. Zhuge Y, Kaufman J, Simeone DM, Chen H, Velazquez OC. Is there still a glass ceiling for women in academic surgery? Ann Surg 2011;253:637-43. 15. Jolliff L, Leadley J, Coakley E, Sloane RA. Women in U.S. academic medicine and science: statistics and benchmarking report 2011-2012. Washington, DC: Association of American Medical Colleges; 2012:1-59. 16. Mayer AP, Blair JE, Ko MG, Hayes SN, Chang YH, Caubet SL, et al. Gender distribution of U.S. medical school faculty by academic track type. Acad Med 2014;89:312-7. 17. Jagsi R, Griffith KA, Stewart A, Sambuco D, DeCastro R, Ubel PA. Gender differences in the salaries of physician researchers. JAMA 2012;307:2410-7. 18. Borges NJ, Navarro AM, Grover AC. Women physicians: choosing a career in academic medicine. Acad Med 2012; 87:105-14. 19. Moss-Racusin CA, Dovidio JF, Brescoll VL, Graham MJ, Handelsman J. Science faculty’s subtle gender biases favor male students. Proc Natl Acad Sci U S A 2012;109:16474-9.

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20. Tesch BJ, Wood HM, Helwig AL, Nattinger AB. Promotion of women physicians in academic medicine. Glass ceiling or sticky floor? JAMA 1995;273:1022-5. 21. Bussey-Jones J, Bernstein L, Higgins S, Malebranche D, Paranjape A, Genao I, et al. Repaving the road to academic success: the IMeRGE approach to peer mentoring. Acad Med 2006;81:674-9. 22. Pohlhaus JR, Jiang H, Wagner RM, Schaffer WT, Pinn VW. Sex differences in application, success, and funding rates for NIH extramural programs. Acad Med 2011;86:759-67. 23. Waisbren SE, Bowles H, Hasan T, Zou KH, Emans SJ, Goldberg C, et al. Gender differences in research grant applications and funding outcomes for medical school faculty. J Womens Health (Larchmt) 2008;17:207-14. 24. Hosek SD, Cox AG, Ghosh-Dastidar B, et al. Gender differences in major federal external grant programs. Santa Monica, CA: RAND Infrastructure, Safety, and Environment; 2005:1-71. 25. Nattinger AB. Promoting the career development of women in academic medicine. Arch Intern Med 2007;167:323-4. 26. Jagsi R, Motomura AR, Griffith KA, Rangarajan S, Ubel PA. Sex differences in attainment of independent funding by career development awardees. Ann Intern Med 2009;151: 804-11. 27. Ginther DK, Schaffer WT, Schnell J, Masimore B, Liu F, Haak LL, et al. Race, ethnicity, and NIH research awards. Science 2011;333:1015-9. 28. Handelsman J, Cantor N, Carnes M, Denton D, Fine E, Grosz B, et al. Careers in science. More women in science. Science 2005;309:1190-1. 29. National Science Board. Science and engineering indicators 2012. Arlington, VA: National Science Foundation; 2012. 30. National Science Foundation, Division of Science Resources Statistics 2008. Thirty three years of women in S&E faculty positions. Arlington, VA: National Science Foundation; 2014. 31. Sheltzer JM, Smith JC. Elite male faculty in the life sciences employ fewer women. Proc Natl Acad Sci U S A 2014;111: 10107-12. 32. Woodruff TK. Sex, equity, and science. Proc Natl Acad Sci U S A 2014;111:5063-4. 33. Kim AM, Tingen CM, Woodruff TK. Sex bias in trials and treatment must end. Nature 2010;465:688-9. 34. Yang X, Schadt EE, Wang S, Wang H, Arnold AP, IngramDrake L, et al. Tissue-specific expression and regulation of sexually dimorphic genes in mice. Genome Res 2006; 16:995-1004. 35. Yoon DY, Manusukhan NA, Stubbs VC, Helenowski IB, Woodruff TK, Kibbe MR. Sex bias exists in basic science and translational surgical research. Surgery 2014;156:508-16. 36. Clayton JA, Collins FS. Policy: NIH to balance sex in cell and animal studies. Nature 2014;509:282-3. 37. Pinnow E, Herz N, Loyo-Berrios N, Tarver M. Enrollment and monitoring of women in post-approval studies for medical devices mandated by the Food and Drug Administration. J Womens Health (Larchmt) 2014;23:218-23. 38. Kim ES, Carrigan TP, Menon V. Enrollment of women in National Heart, Lung, and Blood Institute-funded cardiovascular randomized controlled trials fails to meet current federal mandates for inclusion. J Am Coll Cardiol 2008; 52:672-3. 39. Harris DJ, Douglas PS. Enrollment of women in cardiovascular clinical trials funded by the National Heart, Lung, and Blood Institute. N Engl J Med 2000;343:475-80. 40. Westring AF, Speck RM, Dupuis Sammel M, Scott P, Conant EF, Tuton LW, et al. Culture matters: the pivotal role of

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culture for women’s careers in academic medicine. Acad Med 2014;89:658-63. Demmy TL, Kivlahan C, Stone TT, Teague L, Sapienza P. Physicians’ perceptions of institutional and leadership factors influencing their job satisfaction at one academic medical center. Acad Med 2002;77:1235-40. Lowenstein SR, Fernandez G, Crane LA. Medical school faculty discontent: prevalence and predictors of intent to leave academic careers. BMC Med Educ 2007;7:37. Westring AF, Speck RM, Sammel MD, Scott P, Tuton LW, Grisso JA, et al. A culture conducive to women’s academic success: development of a measure. Acad Med 2012;87: 1622-31. Fried LP, Francomano CA, MacDonald SM, Wagner EM, Stokes EJ, Carbone KM, et al. Career development for women in academic medicine: Multiple interventions in a department of medicine. JAMA 1996;276:898-905.

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45. National Institutes of Health. Research supplements to promote re-entry into biomedical and behavioral research careers. Bethesda, MD: National Institutes of Health; 2010. 46. National Institutes of Health. Research supplements to promote diversity in health-related research. Bethesda, MD: National Institutes of Health; 2012. 47. National Institutes of Health. NIH Policy Concerning Career Development (K) awards: leave, temporary adjustments to percent effort, and part-time institutional appointments. Bethesda, MD: National Institutes of Health; 2011. 48. National Institutes of Health. Research on causal factors and interventions that promote and support the careers of women in biomedical and behavioral science and engineering (R01). Bethesda, MD: National Institutes of Health; 2008. 49. National Institutes of Health. NIH Working Group on Women in Biomedical Careers. Bethesda, MD: National Institutes of Health; 2010.

Gender bias in biomedical research.

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