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      Female rats are not more variable than male rats: a meta-analysis of neuroscience studies

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          Abstract

          Background

          Not including female rats or mice in neuroscience research has been justified due to the variable nature of female data caused by hormonal fluctuations associated with the female reproductive cycle. In this study, we investigated whether female rats are more variable than male rats in scientific reports of neuroscience-related traits.

          Methods

          PubMed and Web of Science were searched for the period from August 1, 2010, to July 31, 2014, for articles that included both male and female rats and that measured diverse aspects of brain function. Only empirical articles using both male and female gonad-intact adult rats, written in English, and including the number of subjects (or a range) were included. This resulted in 311 articles for analysis. Data were extracted from digital images from article PDFs and from manuscript tables and text. The mean and standard deviation (SD) were determined for each data point and their quotient provided a coefficient of variation (CV) as a measure of trait-specific variability for each sex. Additionally, the results were coded for the type of research being measured (behavior, electrophysiology, histology, neurochemistry, and non-brain measures) and for the strain of rat. Over 6000 data points were extracted for both males and females. Subsets of the data were coded for whether male and female mean values differed significantly and whether animals were grouped or individually housed.

          Results

          Across all traits, there were no sex differences in trait variability, as indicated by the CV, and there were no sex differences in any of the four neuroscience categories, even in instances in which mean values for males and females were significantly different. Female rats were not more variable at any stage of the estrous cycle than male rats. There were no sex differences in the effect of housing conditions on CV. On one of four measures of non-brain function, females were more variable than males.

          Conclusions

          We conclude that even when female rats are used in neuroscience experiments without regard to the estrous cycle stage, their data are not more variable than those of male rats. This is true for behavioral, electrophysiological, neurochemical, and histological measures. Thus, when designing neuroscience experiments to include both male and female rats, power analyses based on variance in male measures are sufficient to yield accurate numbers for females as well, even when the estrous cycle is not taken into consideration.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s13293-016-0087-5) contains supplementary material, which is available to authorized users.

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          Female mice liberated for inclusion in neuroscience and biomedical research.

          The underrepresentation of female mice in neuroscience and biomedical research is based on the assumption that females are intrinsically more variable than males and must be tested at each of four stages of the estrous cycle to generate reliable data. Neither belief is empirically based. In a meta-analysis of 293 articles, behavioral, morphological, physiological, and molecular traits were monitored in male mice and females tested without regard to estrous cycle stage; variability was not significantly greater in females than males for any endpoint and was substantially greater in males for several traits. Group housing of mice increased variability in both males and females by 37%. Utilization of female mice in neuroscience research does not require monitoring of the estrous cycle. The prevalence of sex differences at all levels of biological organization, and limitations in generalizing findings obtained with males to females, argue for the routine inclusion of female rodents in most research protocols. Copyright © 2014 Elsevier Ltd. All rights reserved.
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            Studying both sexes: a guiding principle for biomedicine.

            In May 2014, the U.S. National Institutes of Health (NIH) announced that it will ensure that investigators account for sex as a biological variable (SABV) in NIH-funded preclinical research as part of the agency's rigor and transparency initiative. Herein, I describe in more detail the rationale behind the SABV policy component and provide additional detail about policy goals. In short, studying both sexes is a guiding principle in biomedical research that will expand knowledge toward turning discovery into health. NIH expects that considering SABV in preclinical research will help to build a knowledge base that better informs the design of clinical research and trials in humans. Integrating the practice of studying both sexes in preclinical research will, over time, expand our currently incomplete knowledge base that plays a critical role in informing the development of sex- and gender-appropriate medical care for women and men.
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              Twenty years and still counting: including women as participants and studying sex and gender in biomedical research

              Background This paper chronicles attempts in the United States over the past 20 years to fully represent women in clinical trials and ensure the study of sex and gender in biomedical research. We maintain that productive science with the aim of serving the public health requires examining the influence of sex and gender on health outcomes. Discussion This section provides a historical perspective on the changes in recommendations and requirements of both the National Institutes of Health — the world’s largest single funder of biomedical research — and the U.S. Food and Drug Administration — the world’s most influential regulator of drugs and medical devices — for the acceptable conduct of research as it relates to sex and gender. We also cite all reports by the U.S. Institute of Medicine and the U.S. Congress’ General Accountability Office issued from 1990 to the present on the inclusion of sex and gender in research, and selected high-impact published studies that illustrate and document the paucity of, yet the need for, inclusion of females and consideration of sex and gender in research across an array of biomedical disciplines. Summary The key message of this paper is that it has been 20 years since the first requirements to include women as well as men in clinical trials and analyze results by sex were mandated by a U.S. federal law, yet not nearly enough progress has been made. Recent signs of potential change in both policy and practice of scientific inquiry suggest much more progress may be within reach. However, awaiting a cultural shift to allow the study of sex and gender to be embraced is not seen as an effective strategy for change. Rather, specific instrumental recommendations are offered for how to include the study of sex and gender in research so as to increase our understanding and promotion of health for the benefit of all.
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                Author and article information

                Contributors
                jbbecker@umich.edu
                Journal
                Biol Sex Differ
                Biol Sex Differ
                Biology of Sex Differences
                BioMed Central (London )
                2042-6410
                26 July 2016
                26 July 2016
                2016
                : 7
                : 34
                Affiliations
                [1 ]Department of Psychology, Neuroscience Graduate Program, University of Michigan, Ann Arbor, MI USA
                [2 ]Department of Psychiatry, Molecular and Behavioral Neuroscience Institute, University of Michigan, 205 Zina Pitcher Place, Ann Arbor, MI 48109 USA
                [3 ]Department of Psychology, University of Chicago, Chicago, IL USA
                [4 ]Psychology Department, Hunter College, CUNY, New York, NY USA
                Article
                87
                10.1186/s13293-016-0087-5
                4962440
                27468347
                3bed76ef-4025-415a-ac28-ab6b87d3444b
                © The Author(s). 2016

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 13 June 2016
                : 18 July 2016
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000026, National Institute on Drug Abuse;
                Award ID: R01 DA039952
                Categories
                Research
                Custom metadata
                © The Author(s) 2016

                Human biology
                sex differences,sex bias,neurobiology,rattus norvegicus
                Human biology
                sex differences, sex bias, neurobiology, rattus norvegicus

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