Absence of menstruation in female athletes: why they do not seek help

Background It is known that amenorrhea is highly prevalent among female athletes. However, a large percentage of them do not seek help if this complaint occurs. We performed this study to gain more insight into the reasons why female athletes do not seek help when experiencing amenorrhea and how care for these women could be improved. Method Qualitative focus group research. Female athletes were approached to take part in a focus group. They were asked about the main reasons for not reporting amenorrhea and how care for amenorrhea, in their opinion, would ideally be organised. The women were asked to make a list of their top five reasons for both subjects and discuss this among their peers. Results According to the participants, the five main reasons for not reporting the amenorrhea were: (1) normalizing of the subject, (2) the absence of menstruation is not perceived as a problem by the athletes themselves, (3) experienced shame and taboo, (4) prioritisation of sports performance, and (5) denial. Factors to improve care around menstrual cycle problems in female athletes were: (1) informing athletes, coaches, trainers and mentors, (2) informing doctors, (3) conducting more research on long-term consequences, (4) breaking the taboo on menstrual problems, and (5) having a multidisciplinary collaboration between different specialisms. Conclusion By informing athletes, coaches, trainers, and mentors about menstrual cycle problems in athletes, more awareness among those groups can be created. According to the athletes, more research is needed on the long-term consequences of amenorrhea in sports, to enable them to make a better assessment of their possible future health risks. Women experience a taboo on discussing menstrual problems; role models discussing the problem may help in decreasing the taboo. A multidisciplinary collaboration of health care providers may improve care around female athletes with menstrual problems.


Background
More and more women are participating in sports, both at recreational level and professional level. The Olympic Games in Tokyo were the first Olympic Games in which almost 50% of the participating athletes were women [1]. For the last year, there has been an increasing focus on women in sports, including in scientific literature. One of the topics receiving more attention is RED-S (Relative Energy Deficiency in Sport). RED-S was introduced in 2014 and replaces the term 'Female Athlete Triad' . One of the reasons to replace the Female Athlete Triad with Page 2 of 11 Verhoef et al. BMC Sports Science, Medicine and Rehabilitation (2021) 13:146 RED-S, is that RED-S not only involves female athletes, but also male athletes. However, since menstrual problems, both amenorrhea and oligomenorrhea, are one of the most well-known consequences, the syndrome might be easier to diagnose with female athletes than with male athletes [2][3][4].
The etiological factor of RED-S is a low energy availability (LEA), caused by an imbalance between energy intake and energy consumption. A LEA can be the result of disordered eating or eating disorders, but can also occur without disordered eating or eating disorder. The energy imbalance results in a disruption of various physiological functions and systems such as the basal metabolism, menstrual cycle, the (build-up of ) bone density, immune system, and cardiovascular health. The most evident symptoms that can occur are menstrual cycle abnormalities such as amenorrhea or oligomenorrhea. Other symptoms include stress fractures, but also constipation, cardiac arrhythmias, and reduced muscle strength. The exact prevalence of RED-S is unknown. One of the long-term risks is a decreased mineral bone density. Other potential long-term risks are also still largely unknown [5][6][7][8][9][10]. Psychological problems, such as anxiety, irritability and depression play an important part as they can both lead to RED-S and be the result of RED-S. Also, there can be an overlap between eating disorders and LEA; eating disorders can lead to LEA and LEA can also result in eating disorders [9][10][11].
Langbein et al. recently demonstrated the complexity of psychological and physiological interactions of the development of RED-S in a qualitative study among endurance athletes. They also suggested that psychological factors may exacerbate the syndrome or delay recovery [11].
It is known that female athletes underreport menstrual cycle disorders, with a prevalence of up to 40% in some studies [4]. Miller et al. found that 22% of athletes in lean-build sports would not report amenorrhea [12]. In a recent research questionnaire, among female athletes in the fertile life stage in the Netherlands by our study group, 15.6% of all (semi)professional athletes (on average 15 h of training per week) who did not use hormonal contraception indicated that they did not have a menstrual period for the last six months. Of all responders, 31% indicated they would not seek help if they developed unexplained amenorrhea (unpublished results). Several studies have also reported on low awareness among female athletes and their trainer or coaches of the potential healthcare risks that are related to the RED-S syndrome [5,6,13].
This focus group study aimed to gain insight into reasons why female athletes do not seek help with the most evident symptom of LEA; amenorrhea, and what the ideal care for this problem would look like for them. A focus group study design was chosen to explore a wide range of views and experiences on the topic [14,15]. These insights can help to reach this group of female athletes, coaches and sports federations, better in the future and improve the care around menstrual problems in athletes.

Method
For this focus group interview study, we asked women who had previously indicated that they were interested to participate in a study on the topic 'menstruation and sports' . These women had filled out a research questionnaire, focusing on menstruation (disturbances) and sports performance. For this questionnaire, every national sport association recognized by the Dutch Olympic Committee was asked to distribute the questionnaire among their members through their social media accounts, periodical e-mails and websites. In addition, the questionnaire was brought to the attention through social media (Facebook, Twitter, LinkedIn and Instagram). Some (ex-) professional athletes and social influencers were asked to share the questionnaire on their social media accounts as well. The questionnaire was online from January-March 2020.
Women who answered to be interested to participate in further research, were considered potential participants for our focus group study. Potential participants were asked by email to participate in a focus group. Participants were selected based on sports background to provide a diverse range of (endurance) sports backgrounds and ages.
In preparation for the focus groups, an interview guide was developed by two of the researchers (MW and SG). First a brainstorm was held to decide on the two main topics (reasons not to seek help and factors to improve healthcare) and on possible open questions. Next, questions were deleted or rephrased until both researches decided the interview guide was completed [16]. We did not perform a pilot focus group.
All participants gave both verbal and written informed consent and agreed to the recording of the focus groups. The Daily Board of the Medical Ethics Committee of Máxima Medical Centre confirmed that the rules laid down in the Medical Research Involving Human Subjects Act do not apply to this research (METC-number N20.067).
The semi-structured focus groups were led by two of the researchers (MW and SG) based on the predeveloped interview guide (Table 1). MW and SG were instructed by a colleague with extended experience on facilitating focus groups. The groups met online via the web videoconferencing platform ZOOM due to the COVID-19 measures. Participants joined using both video and audio. Participants were not reimbursed for their participation. All researchers and facilitators participating in the focus group were female, to exclude the possibility of participants to feel a threshold to discuss their menstrual cycle due to the presence of a male researcher. No other people besides the participants and researchers were present. In the introduction, the researches introduced themselves briefly, including their name and occupation (SG: gynaecologist, MW: sports physician in training, SV: medical student), their personal sports background and reason to initiate or participate in the research. Furthermore, the goal of the research was introduced. Two researchers (MW and SV) took notes during the focus groups (Tables 2,  3). The focus groups took place in May and June of 2020 and lasted approximately 90 min. The focus groups were audio recorded digitally and transcribed by one of the researchers (SV). The recordings were deleted after transcription was completed. The transcripts were coded using Microsoft Word and Microsoft Excel. The items Table 1 Interview guide Structure of focus group

Introduction
Introduction of facilitator and researchers and their occupation and background, personal interest in sports and explain study goal and basic rules Invitation to the participants to introduce themselves What is your main reason for participating in this focus group? What are the five most important reasons according to you?

Closing and word of thanks
Additional questions to support the discussion Why is this an important feature?
What is the effect of this feature?
Do other participants recognize this point? (top five) of the sub questions were derived from the data and divided into different categories and subcategories by three researchers (SV, MW and SG) based on thematic analysis. Two coding trees were developed (Figs. 1, 2). The focus groups were done one by one until all authors agreed saturation of input was reached. No further repeat interviews were carried out. The COREQ checklist was used to ensure thorough reporting [17]. The main goals of the focus group were to (1) identify reasons why female athletes do not seek help in case of unexplained amenorrhea and (2) to identify factors to improve (health)care for female athletes suffering from these complaints.

Results
A total number of 16 women were asked to participate on the study group. Twelve participants agreed to enter the focus group. The mean age of the participants was 33 years (range 23-45). The participants (previously) practised mainly cycling (n = 6), triathlon (n = 4), speed skating (n = 4), athletics (n = 2), running (n = 2) and mountain biking (n = 1). A number of women (n = 6) practiced multiple sports. Half of the participants (n = 6) were (ex) elite or professional athletes.
A total of three focus groups took place, each with four Dutch female participants. After the third focus group, the researchers decided no new information was provided, appropriate to data saturation.

Reasons for not reporting the absence of menstruation
The five most important reasons for not reporting the absence of menstruation derived from the interviews were (1) normalizing of amenorrhea within surroundings, (2) the absence of menstruation is not perceived as a problem by athletes, (3) shame and taboo, (4) prioritising performance and (5) denial. Each reason is further described below, supplemented by indicative quotes. The quotes were translated from Dutch, with F = focus group number and P = participant.

Normalizing within surroundings
Participants indicated that one of the main reasons for not reporting amenorrhea was normalization by doctors, coaches and other athletes. Some participants mentioned that the general practitioner told them in the past that the absence of menstruation was 'part of exercising a lot' , so these women did not report this complaint to the general practitioner afterwards (F2, P2: "Especially, if you have reported it [the absence of menstruation] and a doctor says that it is okay, then you will certainly never raise the alarm again, even if you do not get it for much longer. "). In addition, these women knew several (elite) Normalizing of amenorrhea within surroundings (21) General pracƟƟoner dismisses amenorrhea in sports (9) Amenorrhea is normal when exercising a lot (6) Amenorrhea is normal if you are thin (1) The menstrual cycle will restore by itself (1) Amenorrhea is no problem except in case of current desire to have children (1) Normalizing amenorrhea by (fellow) athletes (9) This is very prevalent and thus normal among (elite) athletes (8) Reports of professional athletes in (social) media who describe amenorrhea to be normal (1) Amenorrhea is perceived as general sign of fitness by fellow athletes/ coaches (3) Absence of menstruaƟon is a general sign of achieving good form (2) Advise by sports physician to lose weight for beƩer performance and achieve lower fat percentage, absence of menstruaƟon was a sign this was going well (1) Absence of menstruaƟon is not perceived as a problem by athletes (22) Absence of menstrual cycle is probably temporarily and thus perceived as not worrisome (14) Menstrual cycle restored by itself when exercising less during off-season (4) Influence on later life was unknown (3) No current wish to have children (5) Found informaƟon that absence of menstruaƟon is normal aŌer using contracepƟon pill for long Ɵme (2) General health is perceived as good and amenorrhea handy (8) Feeling generally well (4) Absence of menstruaƟon is easy (4) Shame and taboo to discuss the problem (18) Influence of trainer/coach on possibility to discuss menstrual cycle problems (14) Difficulty to discuss with older male trainer/ coach/ GP (5) Perceived threshold of trainers/ coaches to discuss the subject with athletes (4) No influence of gender of coach (3) Fear of harsh reacƟon of trainer / coach (2) Fear and shame (4) Feeling ashamed for underlying (eaƟng) disorder (2) Fear of being seen as less feminine (1) Taboo to discuss menstrual cycle in general (1) Performance is priority (13) Aiming for low fat percentage and beƩer performance (2) The lower the fat percentage, the beƩer the performance (1) A low fat percentage is a sign of fitness (1) Weight gain is unwanted and in conflict with sports performance (11) Advise to exercise less is not achievable/ desirable for serious athletes (2) Fear of lesser performance aŌer weight gain and thus threshold to inform coach (5) Only priority is sports (3) Menstrual cycle is no priority (1) Denial (9) Fear of consequences of visiƟng health care provider (9) Knowing absence of menstruaƟon is abnormal but denying the complaint (4) Avoid advise to change eaƟng behavior or sporƟng regime (3) Avoiding confrontaƟon with health care provider to avoid discussion of food intake (1) Fear of serious diagnosis (1) Fig. 1 Coding tree reasons for not reporting the absence of menstruation Informing athletes, coaches, trainers and mentors (13) Using social media (1) Using online social media or magazines (1) Create awareness with parents and children (3) Informing parents so they can monitor their child beƩer (1) Raising awareness at schools (2) Training of trainers and coaches (9) Organizing course days about the subject (2) Informing trainers and coaches (6) Role for associaƟons (1) Informing doctors (18) Insufficient knowledge physicians (7) No clear answers on quesƟons from athletes (2) Took long before GP took acƟon (2) Different advises from different physicians (1) Gynaecologists do not know enough about sports (1) Sport physicians do not know enough about hormones (1) Knowing when referral is necessary (2) GP should have a red flag list (1) GPs should have more training on the subject (1) Informed physicians can inform athletes beƩer (9) Organizing refresher courses (4) In ideal world all physicians have knowledge on amenorrhea (2) Informing athletes about health risks is important (3) More research on long-term consequences (14) More research on long-term risks (9) Too liƩle research has been done (2) More research on (chances on) long-term risks ferƟlity (5) More research on influence diet (1) Influence of sporƟng on young age (1) BeƩer assessment by being beƩer informed on risks (5) Long-term risks ferƟlity (3) Making potenƟal health risks clear (2) Breaking the taboo (17) Breaking taboo around menstrual problems in general (7) If more people know, the easier people speak (2) Breaking taboo on menstrual cycle (3) StarƟng conversaƟon about menstrual cycle problem (1) Using social media to break taboo (1) Way in which menstrual problems are discussed is important (10) Speaking with coach about menstrual cycle should be possible (1) Easier to speak with female coach or physician (3) Gender of coach or physician does not maƩer (2) Ask athlete if she experiences it as a problem (1) Making it normal for coaches to talk about menstrual cycle of athletes (3) MulƟdisciplinary collaboraƟon between different specialisms (23) Signaling role GP, physical therapists and chiropractors (6) GP as first contact (5) Paramedical care has important signaling role (1) MulƟple specialƟes and paramedics should be involved (17) Involvement of gynaecologists (4) Involvement of sports physicians

The absence of menstruation is not perceived as a problem by the athletes themselves
Another reason was that many participants did not experience the absence of menstruation as a problem. For example, women thought it was convenient and also because they had no current whish for children. (

Shame and taboo
For some participants, shame and taboo played a role. Women were ashamed of not having their period because they were afraid of being judged for a lack of femininity (F2, P1: "That you are judged on that, that it does not happen, that it does not happen, well that something is wrong then because every woman basically gets her period every month and if it does not happen then maybe there is something wrong with your femininity. "). Also, in some cases there was an underlying eating disorder, which was a difficult topic for them to discuss (F2, P1: "That was partly due to sports and partly an underlying eating disorder I developed at the time" … "For me, it was mainly shame at the time why I did not raise the alarm. Because a lot of other things were also involved. "). Several participants experienced a taboo around discussing menstruation (F2, P4: "And I certainly think that talking about it is a taboo. That a lot of women still feel like, I would rather not. "). There were different opinions about the relevance of the gender of the care provider or coach regarding this topic (F1, P2: "Now I have a female general practitioner and before I had a male general practitioner. I found it less pleasant to discuss something like that with a 60-year old man than with a woman. " F2, P2: "I have always had male coaches and I personally do not have a problem talking about that… So I feel like that is a much discussed topic. So whether that is a woman or a man does not really matter to me. ").

Performance is priority
According to the participants, performance is an absolute priority in an elite athlete's life. Therefore, as young adults, they only had an eye for sport (F3, P3: "In an elite sports life or in a phase of that part so to speak, yes, then your goal is to perform… then that is number one. And it really is not anything else. Then you are not concerned with having children or anything else I think. "). According to the participants, performance was also a priority for coaches at the highest level. Therefore, athletes experienced an additional barrier to approach a coach or doctor with any health concerns (F1, P4: "I have to live with it because then I perform better. And if I tell my coach that I have this problem which means I actually have to weigh more, then I will not perform the way I normally would. So of course that creates a huge threshold to present something like that to a trainer or coach. ").

Denial
Some participants knew that a lack of menstruation was not a good sign but did not want to be confronted with this. The elite athletes were afraid that they would have to make adjustments in their diet or training regimen that might worsen their performance (F3, P1: "That you are afraid that if you go to a doctor, that he or she will tell you to change something. So  especially not wanted to hear that I should have gained, say, 5 kilos. ").

Optimization of care around menstruation problems in female athletes
Participants mentioned several factors that could contribute to an optimization of care around menstrual problems in athletes. The five most important factors distilled from the interviews were (1) informing athletes, coaches, trainers, and mentors, (2) informing general practitioners and other health care providers, (3) conducting more research on long-term consequences, (4) breaking the taboo on menstrual problems, and (5) developing multidisciplinary collaboration between different health care specialists. The factors are explained in detail below.

Informing athletes, coaches, trainers and mentors
According to the participants, athletes, coaches, trainers and mentors should all be informed about the significance of absence of menstruation in female athletes so that awareness can be created. For example, athletes could be reached through social media or be educated at schools (especially schools for elite athletes). Informing coaches or trainers during for example course days was considered important because of their signalling function (F1, P4: "Informing coaches, trainers and guidance about this. Those [coaches, trainers] are the people who have to signal it, or at least with whom a cyclist has to feel safe enough to discuss that problem. And that is only possible if cyclists know that this problem has also been mentioned during courses. "). Participants indicated that athletes often feel safe with their coach or trainer, and therefore they should (be able to) start a conversation about menstrual problems. Informing the parents of athletes was also mentioned, because they can monitor the development of their child (F2, P1: "If they [parents] also know more about it, suppose, perhaps, being informed by coaches who indeed know more about it, then they can also keep more of an eye on it. Because they of course see their child every day, so to speak, and they might also talk with them more. ") and identify changes.

Informing doctors
According to the participants, there is still a lot of progress to be made in informing doctors (F1, P1: "I notice that I still have to find out a lot of things myself and then I present it to both my gynaecologist and sports physician, then they will have a look at it. But that there is still a lot of ignorance. " F2, P1: "At the time [of amenorrhea] I was advised by one general practitioner to just take the contraception pill to induce it, and the other general practitioner said 'you actually should not do that, your body should do that on its own. '"), for example, by organizing refresher courses or (additional) trainings about RED-S. Participants expected this would enable physicians to better inform athletes. Some participants indicated that a general practitioner or physician does not need to know all the details about the subject but does need to know when a referral is necessary (F1, P1: "But maybe a general practitioner can have some kind of a red flag list, for when should I refer in such cases.").

More research on long-term consequences
Participants indicated that they would like to be educated on the long-term consequences, especially on fertility (F2, P2: "Because I think I am most afraid that my elite sport would do something to my fertility, yes. Because that is really, yes I would find that very bad, so to speak.").
They indicated that more research should be done on this subject (F3, P3: "When someone comes, what can you tell them? What are the rates of infertility, I am just saying something, how likely is it that the menstrual cycle will just come back?"). According to participants, this would allow an athlete to be better informed and to make a better assessment of the risks (F3, P3: "The ultimate goal is maybe to provide insight into what it can cause or what it can mean for the future, to provide insight into the dangers.").

Breaking the taboo
Participants repeatedly mentioned the importance of breaking the taboo surrounding menstrual problems (in athletes). In part, this could be achieved by making the existence of the problem known to a wider audience (F2, P4: "And the more people know about this, that this is an issue at all, the more people will also be interested in it and will talk about it more easily."). The way in which menstrual problems are discussed with an athlete by a coach or doctor is important according to the participants (F3, P3: "I think the way you start the conversation matters a lot. For example, you can say 'I know of women with a lot of injuries that they very often do not have their periods, that actually happens quite often, is that the same for you?' That is already a different question than simply asking an open question, I think.") to find out how an athlete can be helped in the best way (F3, P3: "That is actually the most important thing, that you start the conversation. What belief does someone have, what idea does someone have about it? I think that is the most important thing.").

Multidisciplinary collaboration between different specialisms
According to the participants, a general practitioner ideally plays an important role in the care surrounding

Reasons for not reporting the absence of menstruation
According to the participants, the main reasons that female athletes with amenorrhea do not seek help were 1) normalization of amenorrhea, 2) not experiencing the absence of a menstrual cycle as a problem, 3) experienced shame and taboo around the subject, 4) prioritisation of sports performance, and 5) denial of the problem. Both normalizing amenorrhea and not experiencing amenorrhea as a problem are vicious circles that can be broken by educating female athletes and those around them about RED-S and the associated potential health problems [6].
Participants indicated that they experience a taboo on menstrual problems. By breaking this taboo, there will be less embarrassment for athletic women to seek help for amenorrhea. Social media influencers and role models could play an important role to achieve this. In recent years, big players like Garmin and Nike have started to motivate women to track their menstrual cycle in their mobile app. This might also lead to more awareness among female athletes.
Failure to ask for help when not menstruating because performing is a priority, is often an incorrect assumption.
RED-S also has negative effects on athletic performance, which can include decreased muscle strength, decreased endurance, and increased risk of injury [6]. Training sessions are also more likely to be cancelled due to injuries, illnesses, or complaints, resulting in a reduced training effort. Also the psychological impairments associated with RED-S will negatively influence sports performance. Thus, by better informing athletes about RED-S, incorrect assumptions and fears can be removed.

Optimization of care around menstruation problems in female athletes
The main factors that participants mentioned for optimizing care around menstruation problems in female athletes were informing athletes, coaches, trainers, and mentors, informing general practitioners and other health care providers, conducting more research on long-term consequences, breaking the taboo, and developing multidisciplinary collaboration between different specialisms.
Little attention is paid to RED-S within international sports federations. In 2017, only 7% of international sports federations had a program or guideline on RED-S or conducted research in this area [18]. The IOC recommended improving awareness of RED-S among athletes, coaches, mentors, and sports organizations [6].
Recently, Langbein et al. have described a qualitative exploration of RED-S in endurance athletes. While their patient population differed somewhat of our population and the study focused on different aspects, they also report on the lack of information received and the need for professional support by the athletes, and emphasize on the importance of well-informed members of the team (parents, coaches, trainers, physicians) surrounding the athlete [11].
As far as is known, no research has been conducted into long-term consequences and fertility. The IOC cited the long-term consequences of RED-S as one of the major gaps in knowledge about this syndrome [6].
For several athletes, a multidisciplinary collaboration between different specialties, including a gynaecologist, sports physician, sports psychologist, and sports dietitian, would be ideal for the care of RED-S. A signalling role is mainly reserved for coaches, trainers, physiotherapists, and general practitioners. Appointing a multidisciplinary team to treat RED-S is also a recommendation given by the IOC [5].

Strengths and weaknesses
This focus group study provides insight into the reasons that female athletes do not report amenorrhea and how care can be improved around menstrual cycle problems. These insights were provided by women of different ages and different athletic backgrounds. The heterogeneity of the participants results in a better generalisability of the results. On the downside, some women shared experiences from the past. It is possible that the taboo on speaking about menstrual cycle disorders they experienced in the past has already decreased somewhat. Also, recall bias might have occurred. Moreover, it is likely that knowledge and experience of doctors and coaches about menstrual problems in athletes have increased in recent years.
Amenorrhea is not the only possible form of menstrual dysfunction in RED-S, also other menstrual cycle disorders such as oligomenorrhea may occur. Furthermore, a range of different symptoms are associated with RED-S. These symptoms were not investigated in this focus group study.
Due to the nature of the recruitment of participants, it is possible we have created a selection bias. Also, we focused mainly on endurance athletes, while RED-S and menstrual cycle problems may occur on different types of sports as well.
Transcripts were not sent to participants for comment and/ or correction, nor were the participants able to provide feedback on the findings. The final manuscript was sent to the participants.

Conclusion
The reasons that were given by the participants for not reporting the absence of menstruation are (1) normalization within the environment, (2) not perceiving the absence of menstruation as a problem by the athlete, (3) perceived shame and taboo on the subject, (4) prioritisation of sports performance, and (5) denial.
Several options to improve care around menstrual cycle problems in athletes emerged from this study. More awareness may be created by informing athletes, coaches, trainers, mentors, and sports associations. General practitioners and other health care providers should receive additional training to better inform athletes. In addition, more research on long-term consequences (especially fertility) will help athletes to make a better assessment of the risks in the future. Finally, the care of RED-S can be improved through a multidisciplinary collaboration between different specialties and paramedics. The Máxima Medical Centre has now started a monthly multidisciplinary consultation with sports physicians, sports dietitians, and gynaecologists on women with these complaints.
Abbreviations RED-S: Relative energy deficiency in sport; LEA: Low energy availability.