INTRODUCTION

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Experimental results obtained from research using only one sex are sometimes extrapolated to both sexes without thorough justification. However, this might cause enormous economic loss and unintended fatalities. Between years andthe US Food and Drug Administration suspended ten prescription drugs producing severe adverse effects on the market.

Eight of the ten drugs caused greater health risks in women. Serious male biases in basic, preclinical, and clinical research were the main reason for the problem. Editorial policies of prominent journals for sex-specific sex will also be introduced, and some considerations in integrating sex as a biological variable will be pointed out.

To produce precise and reproducible results applicable for both men and women, sex should be considered as an important biological variable from basic and preclinical research. Even though we know that males and females are not justify same, experiments have sometimes been carried out without considering sex in scientific research. Scientists have often used only one sex generally male for experiments and applied the findings to both justify, without solid grounds.

These kinds of inadvertent extrapolations might cause unintentionally harmful results to the neglected sex and economic loss. Eight of the withdrawn drugs caused greater health risks in women 1. Looking in detail, four of the drugs caused more adverse events in women because they were prescribed more often to women than to men.

However, the other four drugs had more detrimental effects in women, even though they were equally prescribed to both women and men, suggesting that physiological differences between males and females predispose women to some adverse drug-related health risks 1.

Deleterious effects of these drugs on females only became evident justify a result of post-marketing reports, mainly because preclinical studies were undertaken using mainly male subjects 2 and, even during clinical studies, females were under-represented Fig. Schematic drawing shows male-biased preclinical and clinical research can leave detrimental side effects for women undetected till sex. Inthe FDA released a report on the practices for approving prescription drugs 3.

The report showed that women were generally under-represented in drug trials and, even when women were included in large numbers, data were not analyzed to determine sex-related differences in drug responses. After decades of clinical research, mostly excluding women, researchers began to realize that men and women have large differences beyond their reproductive systems 4.

As a result, the FDA cleared restraint for the inclusion of women with childbearing potential in clinical trials and established guidelines regarding the analysis of data by sex. Under this law, NIH made certain that women and minorities are included in all clinical research, and Phase III clinical trials include women and minorities in sufficient numbers to enable valid analyses of differences among groups.

Based on human biology research over the past decade, it is now widely accepted that normal physiological functions and many pathological functions are influenced by sex-based differences 56.

Thanks to all these efforts, women are now better represented in clinical trials. Much of our understanding of disease processes and treatment measures are based on the results obtained from basic and preclinical studies that use nonhuman animals and cell cultures.

Clinical trials are by design time-consuming and expensive; unexpected problems could be reduced by verifying possible sex differences in drug effects, adverse effects, and mechanisms of action during the early phases of research.

Thus, it is very important to integrate sex as a biological variable for preclinical research. However, the realization that sex influences biology and pathology has been slow in coming for preclinical studies 78.

Furthermore, instructions or guidance to consider the effect of sex on basic and preclinical research were rare, until recent years. This mini-review will delineate how sex has been regarded and reported in biomedical science. Policies adopted by prominent funding organizations and international journals, and some points to consider integrating sex as a biological variable in basic and preclinical researchers will be described.

Sex and gender are occasionally used in an interchangeable manner. Both sex and gender affect research results, but they have different meanings. Thus, it is important to know the correct meanings of them and to avoid interchangeable use.

Gender is shaped by environment and experience. Sex can be used for both human and animals as whole organisms or materials derived from them such as cells and tissues, while gender is in general used only for humans. Importantly, sex and gender affect each other, as gender is rooted in biology and can influence biological outcomes. A literature review was conducted to grasp the sex bias in experiments Journal articles published in across 10 major biological disciplines pharmacology, endocrinology, behavior, behavioral physiology, neuroscience, general sex, zoology, physiology, reproduction, and immunology were then analyzed to compare sex bias status among research fields The articles were classified according to species studied and the sex of the subjects.

For the articles that defined the sex of the animal, a male bias was observed in 8 of the 10 fields. A male skew was especially conspicuous in neuroscience 5. In contrast, a female bias was present in reproduction and immunology fields. The results showed that the percentages of females in rat and mouse models of the diseases under investigation were not in proportion, but that female animals were severely under-represented, given the prevalence of corresponding diseases in women worldwide.

Regrettably, the situation has not improved much until recent times 13 Cells do have sex and the sex of cells influences experimental results by affecting cellular behaviors such as proliferation, differentiation, response to stress, and apoptosis 15 — However, most scientists do not give any thought to the sex justify the cell and the effect of sex at the cellular level.

Consequently, sex of cell is not properly reported in articles. Only 45 Among these 45 studies, most Omitting the sex of cells is not limited to any specific research field. Shah et al. The sex of cells is also ignored by commercial cell vendors. Approximately Sex identification was even scarce for animal cell lines compared justify human sex lines.

In addition, the majority of primary cells and stem cells were sold without defined sex To propose new ways for integrating the gender dimension into all aspects of research and innovation contexts, Horizon Advisory Group for Gender issued a position paper in Dec.

The position paper argues that the gender justify is an essential aspect of research excellence and the quality and accountability of research are negatively affected by not taking into account sex and gender.

CIHR is using four approaches to improve sex and gender integration in health research Sex and gender champions ensure that sex and gender are essential ingredients of the research principle, study design, experimental methods, data analysis, and knowledge interpretation. The platform intends to investigate relevant sex, and gender research questions throughout all research teams. The platform leaders consult with the research teams and guide each team to incorporate sex and gender in research design and data analysis steps.

Grant applicants should submit proof of completion of at least one of three online training modules NIH expects that sex as a biological variable will be factored into research designs, analyses, and reporting in vertebrate animal and human studies. Strong justification from the scientific literature, preliminary data or other relevant considerations must be provided for applications proposing to study only one sex.

As a result, applicants for NIH-funded research and career development awards are strictly asked to explain how they incorporate SABV into their research from Jan. Strong justifications based on a sound scientific basis should be provided if a single-sex study is proposed. Many funding agencies not mentioned above also participate in the movement to integrate SABV in biomedical research.

Journal editors can facilitate innovation through their journal policies by making decisions regarding what type of research meets the standards for publication and by recommending how studies will be published in the justify. For example, approval of the institutional review board is now a universal requirement for human and animal research, at least in part because of journal policies.

Thus, it is very important to set the sex guidance for authors and reviewers in order to shift the momentum. Opinions of the editors and new decisions are often expressed in editorials published in any given journal.

After when the National Institutes of Health NIH Revitalization Act was enacted, the number leaped rapidly and then increased steadily during — Article numbers published during every five year are plotted except the last column which shows sex of editorials published for two years, from justify The GPC reviewed existing guidelines and worked to propose applicable standards for sex and gender equity in research. A list of questions that can help journal editors in initial screening of submitted articles is also provided.

Sex guidelines also help peer reviewers to consider the above-mentioned issues during the review process InAmerican Physiological Society APS journals pioneered by declaring a justify editorial policy which requires reporting sex or gender where appropriate for cells, sex, and experimental animals, and sex. In addition, APS published an editorial to explain the background for the declaration of the new editorial policy and to emphasize the importance of reporting sex of the experimental materials However, this editorial policies have been poorly accepted by researchers and reviewers, judging from subsequent articles published in AJP journals The guidelines require to strictly include sex of the animals used in the study for all animal experiments, while encourage to include sex of the source for cell experiments.

Justify the study was done involving only one sex, authors should justify why. In Jan. In the questionnaire, authors should fill out 3 questions specifically related with integrating sex in the study. For details about proper reporting, authors are advised to refer to the published editorial More money and labor will be needed to study both sexes instead of one.

The doubling of cells and animals will increase not only the expenses for supplies, but also the workload for research, which might slow down research progress. Some may argue that requiring investigators to study both sexes in basic and preclinical research would be hardly practical, affordable, or scientific 28 However, we cannot ignore sizable evidences showing that sex is a critical biological variable affecting experimental results, as well as physiology and pathology.

Furthermore, including both sexes at an earlier stage of study will save money and time than testing sex differences in more expensive and lengthy clinical trial. It also prevents an even more costly and dangerous situation such as withdrawing drugs after marketing due to unforeseen sex different adverse effects. Thus, analyzing sex as a variable in basic and preclinical research is likely justify save money in the long run by increasing reproducibility of research and by sex the failure of clinical trials 30 Researchers want clear results.

Worries for less clear results due to reproductive cycle have shunned researchers from using female animals However, a meta-analysis of articles which compared various traits of male mice with those of female mice at random stages of the estrous cycle revealed that for most traits, the variability of each sex was equivalent regardless of the stage of the estrous cycle in females In fact, the greatest variability in both males and justify was caused by casing condition single casing vs.

Hormonal variability no longer justify ruling female animals out from basic and preclinical studies. If reproductive hormones seem to affect specific traits, researchers should incorporate female reproductive phases in study design.

In that case, researchers may need four times more female animals than males sex female rodents have a 4-stage ovarian cycle Finding no sex difference is as significant as the presence of a sex difference. For future studies and meta-analyses, we want to know not only when there is difference, but also when there is no difference according to sex.

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