PAG over Pastries
A pediatric and adolescent gynecology review podcast. Started by a fellow for residents, fellows, and others to learn more about PAG topics.
PAG over Pastries
6 - Relative Energy Deficiency in Sports (RED-S)
Dr. Susan Kaufman is joined by Dr. Mary Romano, a PAG physician from Vanderbilt and the current president of NASPAG, to discuss Relative Energy Deficiency in Sports (RED-S) previously knows as the Female Athlete Triad.
Outline:
• Highlights of a case study involving a 17-year-old athlete
• Identifying high-risk sports for developing energy deficiency
• Psychological and physiological impacts of inadequate energy
• Importance of early detection and intervention strategies
• Key roles of nutrition and hydration in athlete health
• Holistic approaches to treatment, involving multiple disciplines
• Empowering parents and coaches to support athletes effectively
• Importance of addressing hormonal imbalances with appropriate therapies
References:
- NASPAG Essentials of Pediatric and Adolescent Gynecology: Chapter 13
- Reproductive Health Management of Female Adolescent Athletes With Relative-Energy Deficiency in Sport by Mary Romano and Amy Sass in Journal of Pediatric and Adolescent Gynecology
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What is PAG?
Pediatric and Adolescent Gynecology is a subspecialty of OBGYN (2 year fellowship) focusing on reproductive healthcare for children and young adults. It fills the overlap between general gynecologists and pediatricians. It is a multi-disciplinary field involving work with pediatric endocrinology, dermatology, hematology, surgery, ect. Go to NASPAG.org for more PAG educational resources.
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So we have a 17-year-old high school student who presents with secondary amenorrhea. Menarche was at age 14, and her periods occurred every 50 to 90 days until they stopped, and her period stopped about six months ago. She denies any acne or hirsutism. Her BMI is 18. She is applying to college and currently she plays on three varsity teams in high school. I'm Susan Kaufman and I'm a pediatric and adolescent gynecologist at Virtua Health in New Jersey.
Mary Romano:I am Dr Mary Romano and I am an adolescent medicine physician who is part of the division of adolescent medicine at Vanderbilt Children's Hospital in Nashville, Tennessee and it's wonderful to be recording with you today.
Susan Kaufman:We are using Chapter 13 from the NASPAG Essentials of Pediatric Adolescent Gynecology and also an article written by Dr Mary Romano and Dr Amy Sass that's going to be published in JPAG soon and that is entitled reproductive health management of female adolescent athletes with red s in sports. What is your favorite pastry?
Mary Romano:I live in tennessee, it's hard to come by a good new york italian pastry like I used to, so I'd go with linzer tort, what about you?
Susan Kaufman:I am not familiar with that. I'll have to look it up.
Mary Romano:You know powdered cookie jelly.
Susan Kaufman:Well, chocolate all things chocolate and chocolate cake is on the top of my list. M ary take it away.
Mary Romano:so we are going to talk about relative energy deficiency in sports today also known as Red S. It used to be, or was previously known as, female athlete triad. In 2014, the International Olympic Committee issued a consensus statement outlining and expanding the female athlete triad to encompass Red S, and the reason for doing that was I guess there was a few reasons that they did that. One was to reflect that it doesn't only occur in females, it occurs in males as well. It also reflected the fact that it occurred along a spectrum.
Mary Romano:So the female athlete triad, which referred to osteopenia, disordered eating and amenorrhea, was really the endpoint of relative energy deficiency in sports. And what you really want to do is pick up someone like this athlete that we're going to talk about today, who perhaps doesn't quite have severe bone health deficiencies, doesn't have complete amenorrhea, but perhaps is starting to move in that direction. And then the other thing the new diagnostic criteria did was to reflect on the fact that it doesn't just affect bones and periods. Those are probably the things we think about the most and we worry about the most, but it mentions, or it sort of wants us to be aware, that it affects all systems of our body right Our immune system, our GI tract, our endocrine system, our metabolic system, our hematologic system and that there are significant psychological effects beyond those who carry a frank diagnosis of a DSM-5 eating disorder.
Susan Kaufman:Exactly, and we're going to be posting a chart from Mary's article on the website with the transcript of this podcast, and the chart shows us all of the different systems that are affected and it just organizes it so nicely. So if you go on the website you'll be able to find that. Can you define for us energy availability?
Mary Romano:Of course and that's a term you'll see us use a lot when we take care of these athletes.
Mary Romano:So energy availability in anyone is what we use to define what energy is left for your body to do the things it needs to do, based on what you take in and what you put out.
Mary Romano:And so you can imagine, we all have an element of energy availability, but in athletes, particularly elite athletes or multi-sport athletes, it is going to take a lot of energy in to match all of the energy they expend out, and so for some athletes, unintentionally, they may just not realize how much they need.
Mary Romano:We actually know that exercise in the immediate period after you exercise can suppress your appetite. And for some athletes, unfortunately, who may have a DSM-5 diagnostic restrictive eating disorder, such as anorexia nervosa, there may be an intentional plan to restrict their energy relative to what they put out, because they're either trying to change their weight or maintain a certain weight that they perceive to be healthy and the best for their sport. So that energy availability is critical in assessing what does this athlete have available to them to participate in their sport but also maintain their essential bodily functions, like building strong bones, like having adequate function of all of your systems and then, obviously, to have normal ovulatory menstrual cycles. And it would be interesting to know, susan, what athletes are at the greatest risk of developing red S, because certainly you can anticipate that some would be more at risk than others?
Susan Kaufman:Right, but we also have to keep in mind that it's not only our highest level athletes, but people who engage in sports on a casual basis can also develop red S and some of the sports we see it more commonly in our track, especially our long distance runners. Because they are encouraged to have a lean body mass, they may restrict their food intake and with their energy output, it causes an imbalance in their energy availability. We can see this in our dancers. We can see this in our gymnasts. Again, it's all about body image and being encouraged to maintain lean body mass. It can occur in any sport, but I had a college level basketball player who developed red S because she was trying to keep her weight under control and she thought that would help her perform better in her sport. So we have to be aware that it can involve any sport.
Mary Romano:I know we're gynecologists, but another sport to think of when we think about male athletes is wrestling. Right, so often wrestlers have to make a particular weight class, and so they may have intermittent disordered eating to like make the weight class right before the meet, or they may chronically engage in restrictive eating behaviors in order to keep themselves in that weight class.
Susan Kaufman:That's important to mention because now there are high schools and colleges that are starting female wrestling programs
Mary Romano:my daughter plans on joining one
Susan Kaufman:okay! and especially the folks that wrestle in the much lower weight classes, which may be a weight that's actually too low for their height. In addition to endocrine and bone and cardiac and psychological effects, we of course are concerned about menstrual effects, and a lot of times these young women initially present with absent periods, and that's our first clue that there is something going on. The energy deficit will interrupt the pulsatile GNRH output from the hypothalamus, leading to decreased FSH and LH and decreased estradiol from the ovaries. And why is decreased estrogen production in these athletes a concern?
Mary Romano:So it's certainly a concern, because we know that estrogen, or estradiol, is the hormone that is not just responsible for ensuring regular ovulatory periods, but it's also the hormone that's responsible for promoting bone health. So estrogen is important in bone development and it's really critical to make sure we maintain a healthy balance between bone building osteoblastic activity and bone removal osteoclastic activity yeah, so bone modeling and so what we always, you know, remind athletes it's not just what your bone looks like. Right, you can have a styrofoam bone and you can have a steel bone, and they're going to look the same, but they're going to be very different in terms of their bone density and having adequate sex steroids in general. So testosterone as well is going to be important for having strong bones and healthy bones and bones that can sustain prolonged periods of weight-bearing exercise.
Susan Kaufman:So the lack of estrogen will not only lead to absent periods and genital atrophy and maybe some bladder dysfunction. It can affect their skin. A lot of these folks describe foggy brains, so they get some of the symptoms that perimenopausal or menopausal women might have because of the lack of estrogen and of course we're concerned about all of that. But we also have parents that are concerned about future fertility when they bring their daughters in and say my daughter's not getting her period. Also, red S can affect thyroid dysfunction. We can see something called sick thyroid euthyroid, where the thyroid has the ability to function normally but it is not because of the suppression that's going on with the energy imbalance. Also, insulin secretion can be affected and growth hormone can be affected and we may see elevations in cortisol which may further impact lack of bone building, again because of the hormone imbalance.
Mary Romano:The goal is to pick up these athletes before their moms bring them in and say, hey, they have no period, right?
Mary Romano:The hope would have been that this athlete that we're talking about in this case, that someone would have picked up on the fact that she only gets a period every 50 to 90 days and said, hey, after two years post-menarche, that's not appropriate, that's not normal.
Mary Romano:And so you, you want to start to sort of look at the energy availability in these girls before they get to frank amenorrhea.
Mary Romano:And I think the other thing you have to - and fight is probably too strong of a word with these girls is they're going to be elite athletes that are living in a culture where you may even have moms who were, like I was a track athlete, I never got my period during the track season, and so it's also important to make sure that we educate coaches and trainers and parents to say you may have an entire team of athletes who don't have regular periods.
Mary Romano:That doesn't mean it's normal, it means that there is an issue with everyone's energy availability, and so certainly it can be a challenge when you're sort of making treatment recommendations If you're also butting up against, or butting against a culture that doesn't think it's abnormal to have an irregular period pattern in the context of a significant amount of exercise. So you want to make sure that that education occurs, both for parents, providers, coaches because you're also often dealing with scholarship athletes. So there are financial implications and it's a lot to kind of it's a lot of it's a very global and comprehensive conversation that needs to occur.
Susan Kaufman:The other thing is a lot of the athletes don't want to get their periods because it interferes with their sport. You know they have to use pads, they have to use tampons. They may not feel good when they get their period, they may have some PMS, they may feel tired. So that's another encouraging quote-unquote aspect of this, that, oh, I'm not getting my period now. This is great, this is better. And it's sometimes hard to convince them that their performance is actually impaired when they have red S.
Mary Romano:Luckily there have been a few professional athletes that I think have been more outspoken about normalizing period discussions in sports, which has been wonderful.
Susan Kaufman:So what do you do with somebody who comes in and they're either not getting periods at all, or their periods are very irregular and they're involved in any sport that we mentioned?
Susan Kaufman:How do you go from there.
Mary Romano:So one of the first things we always look at is growth charts. So is this an athlete who's always lived at a inappropriately low BMI? Is this an athlete who used to live at a higher BMI and gradually over the years has drifted downward? So it's always helpful, if you're a referring provider, to have access to growth charts and then, honestly, it's really about having a conversation with that athlete and you know it sounds silly, but we sort of sit down and say talk me through a day of eating.
Mary Romano:You wake up, what is your breakfast, what is your snack, what is your lunch, what is your dinner? And, like all things in medicine, it's important to be very specific, because an and strawberries, and if you sort of drill that down into, well, tell me exactly what that looks like. It's a low carb wrap with one slice of turkey and three strawberries. So you know we always say that healthy eating has to have quantity, quality and flexibility. So we want to make sure you literally eat enough that you're getting in all the food groups. So some athletes will eat voluminous amounts of food, but it's only vegetables and they don't do carbs. And we know carbs are an essential part of a healthy diet, contrary to what society may tell us and flexibility. Is this an athlete who will eat four things all day, every day, and is unable to fuel her body when the team travels for a spring break and they have to eat Taco Bell at a rest stop? So you want to really make sure you deep dive into how they're fueling their body, and with specific information.
Susan Kaufman:And drilling into their exercise. So if I'm talking to somebody who's running track, I really want to know how many days a week are you running, how many miles are you running when you're training? Because they'll just tell you oh, we just, you know, I run a few days a week. Well, what does that really look like?
Mary Romano:I should have said that as well. A history of bone stress injuries. So is this an athlete who's had multiple stress fractures, multiple bone stress injuries, which again were normalized in an elite athlete? That is a sign that that body is under stress.
Susan Kaufman:Right, and also one other thing I thought about with the diet history is to delve into whether they're getting enough calcium and enough iron in their bodies.
Mary Romano:Absolutely, and vitamin D.
Susan Kaufman:So what about lab tests?
Mary Romano:Right. And so you know, the amenorrhea that we see in athletes with S is is known as functional hypothalamic amenorrhea or FHA, and it's a diagnosis of exclusion. So, I also believe in either the chapter of the article, there's a great chart that we adapted from previous articles that go through that. So I always sort of tell athletes and parents we are getting labs for two reasons right. One is to make sure there is not a medical reason that you're either losing weight, unable to maintain weight or not getting a period. And then we're also getting labs to look at the potential consequences of malnutrition.
Mary Romano:So you're doing things like getting a complete blood count with a differential. You're checking their thyroid function, you're checking their liver function, you're checking their kidney function to make sure you're not missing something like Addison's disease. You're going to dip a urine to make sure this person doesn't have renal tubular acidosis or new onset diabetes that's gone undetected.
Susan Kaufman:Or pregnancy
Mary Romano:Pregnancy, yep, pregnancy. You may be doing an HIV test to make sure that in someone who's sexually active that they haven't acquired an STI.
Mary Romano:And we often will do a SED rate to make sure that we're not missing some kind of inflammatory bowel disease or celiac disease. If someone has significant GI complaints. You may also be getting a celiac screen as well. So again, you want to make sure that. And the other thing to keep in mind is people can have both right, you can have celiac disease and an eating disorder and red S. You can have diabetes and red S. So you're sort of looking for both things and often in athletes with red S, what you're going to find as you go down the algorithm is that almost everything is negative. If you were to check as you would an FSH or an LH or an estradiol, because you may be looking also for premature ovarian insufficiency or a DSD again, you're kind of casting your net wide.
Mary Romano:Often these patients have low FSH and LH and they will have low to undetectable estradiol levels
Susan Kaufman:Right and if we're going to really rule out other hormonal issues, we should get a total and free testosterone and a DHEAS. Sometimes I will get an ultrasound because I want to see if they're building up any lining whatsoever in their uterus, because it's another argumentative point. I have to support the low estrogen level.
Mary Romano:Sometimes actually have to get ultrasounds because, you know, we think of secondary amenorrhea, because we think of someone who perhaps developed red ass later on in life. I've actually recently have had my fair share of elite athletes who have primary amenorrhea, so who have been elite athletes at such a young age that they never had menarche and so oftentimes, like anyone who has primary amenorrhea, you may be getting an ultrasound to make sure that their mullerian structures are present, intact, normal, pre-pubertal, post-pubertal, and making sure there are no anomalies there or structural anomalies that are causing their menstrual irregularities.
Susan Kaufman:Absolutely. Now what about a physical exam?
Mary Romano:So I think the first thing is vital signs, right? So we said the period is a fifth vital sign. So obviously LMP should always be documented. And then we're looking at heart rate and this can be a challenge, right?
Mary Romano:So often in patients with restrictive eating disorders and low energy availability, you will see bradycardia. However, if you're an elite athlete who also runs track, there is an element of normal bradycardia. So it's often important to talk to the coaches, to talk to sports medicine doctors, to say, hey, in an athlete who engages in this sport with adequate energy availability, what would be an expected heart rate? You're going to look at blood pressure because you may see hypotension. You're going to look at temperature, because you may see hypothermia in patients with significant low energy availability. So vital signs is often going to be your first clue.
Mary Romano:In patients who are purging, you can see callusing of their knuckles from repeated purging. You can see parotid enlargement or changes in their teeth. You may also see changes to their skin. So some patients with chronic low energy availability will have a soft layer of hair called lanugo. Some patients who are eating high amounts of beta carotene vegetables like sweet potatoes and carrots, may have actually an orange hue to their skin. Conversely, we've had patients that have had Addison's disease, that are tan in the middle of winter. It's very possible that their exam is totally normal and then obviously you're going to do when the patient consents to a GU exam. You want to make sure there's nothing on GU exam that points to another cause. So do they have an imperfect hymen? Do they have clitoromegaly, which may be a sign of hyperandrogenism? In someone that has Red S, you see signs of estrogen deficiency and atrophy.
Susan Kaufman:Once we get to the diagnosis of Red S, then is there any other testing we want to do before we start talking about therapy. So one of the other studies that I will get is a bone density study.
Mary Romano:Yeah, so I mean, typically the recommendation is if you've had amenorrhea for more than a year you should get a DEXA scan. There are also recommendations for DEXA scans based on the number of bone stress injuries you've had and where you've had them. Unfortunately, there are no formal recommendations for DEXA scans in patients who have primary amenorrhea. So often those patients automatically get a DEXA scan because we have no idea where their baseline is. And I think the important things to remember when you get those DEXA scans is that in adolescence we use Z scores and not T scores, because that's the data that's normalized to that age group. And reminding athletes that their criteria for osteopenia and even osteoporosis is set higher than non-athletes, because we would expect athletes that engage in weight-bearing sports to have a higher bone density at baseline. So that may be confusing to them because the person who reads their DEXA scan may say it's normal and then we have to put that information in the context of well, you're an elite athlete and your bone density should be here higher than what is expected for normal.
Susan Kaufman:Right, let's move on to treatment.
Mary Romano:Yeah. So I mean, I think, like all things in medicine, it's got to be a personalized approach, it's not a one size fits all. What you're hoping to do in your interview with the patients is really get a sense of why they're not meeting their energy needs. So are they just completely unaware of how much they need to eat? And if that's the case, then the treatment may merely be that they need to go see a sports dietitian with some experience treating patients with eating disorders. But really, you want a dietitian that's comfortable with athletes. Who is going to give this patient a prescription, right? So I tell patients, if you're not getting your period due to low energy availability, your medicine is food.
Mary Romano:Obviously, if in those athletes we get pushback, they seem to have an inability to meet those needs, we may need to pivot and think about other therapy modalities In patients where it's relatively obvious that, hey, this person has an eating disorder. So you want to be seen by a medical provider that has experience with caring for patients with eating disorders. Knowing that it's going to be a team approach, right, they're going to need to see a dietician who has expertise in athletes and caring for patients with eating disorders. Then I want to see a sports medicine physician who often is helping navigate bone stress, injuries and limitations that may be placed on their athletics based on that, and then there's typically going to be some kind of therapist.
Mary Romano:It may be that that person just needs therapy to process distorted body image, the stress that will come with perhaps limiting the athletics that is so important to them. And then there may be patients in whom there's concurrent depression, anxiety, ocd, other diagnostic mood disorders, and then they will often have a therapist that has to, in addition to dealing with the body image aspects, address the mood disorder and certainly for patients with a mood disorder there may also be a role for a psychiatrist to discuss psychotropic medication. It is hard to assess for a mood disorder in someone that has a malnourished brain. Malnourished brains are anxious and irritable and perseverative and depressed, and so we may sometimes wait to make that diagnostic or that therapeutic recommendation until there's adequate nourishment to truly assess what their mood is like when their brain is adequately fueled.
Susan Kaufman:Right, and we also have to be careful about how we approach all of this. We can't just dump all of this at one time on the patient, because they're just going to tune out and you know.
Mary Romano:And walk their head might explode
Susan Kaufman:Right and never want to come back to our office. So, absolutely starting with nutrition first of all, and maybe starting with some therapy to help them accept what's going on with their bodies, Just as a final therapeutic measure, we may have to supplement iron. We may have to supplement vitamin D and calcium.
Mary Romano:The only other thing I was going to add on. It's important to loop in parents. There may be certain instances where patients really feel like parents are not an appropriate resource, but when it is possible, I think it is critical with your college student to get Thank you their parents support
Susan Kaufman:also because the parent may be playing a part in this. You know the parent may be pushing this person to continue their athletics and not understanding why they have to stop. And if they're college students, that scholarship is so important. And if they're high school students working towards a college scholarship or wanting to get into a D1 school.
Mary Romano:And it may be a financial necessity, right, I mean, that may be the only chance this child has of attending or completing college, and we don't want to devalue or underestimate how important that's going to be as well.
Susan Kaufman:So we've talked a lot about therapeutic intervention and the last part of that to mention is estrogen therapy. We want to save that to last because we really hope that nutritional changes will improve the red ass situation. But if it does not, or if we have a young woman with severe lack of bone building, then we're going to start estrogen therapy. We prefer to use estradiol as opposed to the synthetic estrogens that are in a birth control pill, unless somebody needs a birth control. But we'll use estradiol and the best way to give it is in a patch and it's giving the patient a natural estrogen.
Mary Romano:I think what we try to stress is that oral estrogen seems to suppress other bone trophic hormones, and so we really want to avoid oral estrogen. Because of the way it's metabolized, it actually it seems counterintuitive, but it can do more harm than good because it affects other bone building hormones that your body makes Sometimes.
Susan Kaufman:I will start out on much lower doses than this person actually needs, primarily to show them that they can tolerate it and they won't have side effects, and try to get them up to a higher dose as soon as possible, and the goal, basically, is to get them to a 0.1 milligram patch.
Susan Kaufman:And then the question comes up about progesterone.
Susan Kaufman:When do we add it, what do we add and how do we add it? So, classically, the teaching is to use a cyclic progestin. The micronized progestin is the most commonly used. But frankly, I think that's a shared decision making situation with the patient and if I have a patient who absolutely does not want her periods back, then I'm going to use continuous progesterone. Know that treating the amenorrhea in a continuous fashion is going to mask some of the recovery markers we're looking for, but again, it's a compromise. But I won't start those until I have signs that a lining is being built up. So maybe when they start having some bleeding, then we'll start progesterone.
Mary Romano:We often follow estradiol levels right.
Mary Romano:So for most of these athletes, when we're having a discussion about starting the transdermal estrogen, their estradiol levels are undetectable and so we're really looking to move it into a detectable range. I will also say it may take a while for these athletes to have a regular cycle. So even if they're not using the transdermal estrogen, if their estrogen levels are moving from an undetectable level into a more normal physiologic range, that is still a marker of recovery and you can sort of utilize that to make adjustments to training and activity and to intake, because we know from a bone health perspective that we're protecting them with adequate estrogen levels. We do know that data would say to reverse all of the effects of an eating disorder the cognitive effects, the GI effects, all the things you do have to have a regular period. That is a critical part of recovery. But for some of these athletes that will take a very long time to happen. So as long as you're moving their estradiol into a physiologic range, you're at least achieving that bone health protection which is one of our main goals.
Susan Kaufman:Correct. I think the longer they have been suppressed, the longer it takes for their ovaries to recover.
Mary Romano:The IOC released its guidelines in 2024. One of the things they did with those updated guidelines is that they created wonderful tables and algorithms for how you can think about the safety of participating in physical activity. They have this very visual red, yellow, green, and so that CATS tool is very helpful in categorizing the severity of the eating disorder and then helping guide practitioners in that return to play and it's, you know, evidence-based. So it's not like well, dr Kaufman said I could do it when I got to got to this weight and dr Romano said I could do it when I ate five times a day. This is a very evidence-based, very concrete and visual, which I think is wonderful.
Susan Kaufman:Right, and we'll put that chart on the website as well.
Susan Kaufman:To sum up where we are...?
Mary Romano:Absolutely. So, if you go back to the case you started with in this 17 year old, we need to ask a lot more questions because on the surface, this girl would appear to have lots of risk factors for RED S, right. She's a multi-sport athlete, she's a senior in high school, we're going to imagine that comes with a significant amount of stress, and so you're certainly going to want to screen her carefully for red ass and make sure that you figure out what's going on with her periods, even if you decide that in that moment that's not what's going on, that you continue to follow her closely to make sure that her weight trajectory, her menstrual trajectory, her nutritional trajectory all stay on track.
Susan Kaufman:Exactly, and that takes also educating the coaches and everybody from the high school level up involved with these young folks. Okay, well, this is going to conclude PAG Over Over Pastry podcast on Red S, and we hope that you have enjoyed this and you'll get some great takeaway messages from this. Dr Romano, thank you so much for joining us today.
Mary Romano:Thanks so much for having me.
Mary Romano:Thank you for taking the time out to talk about this really important topic.
