The Dangers of Underfueling for Endurance Athletes

Introduction

In a previous article, we shared about foundational nutrition for uphill athletes, introducing the Athlete’s Nutrition Pyramid to clarify nutrition priorities. At the pyramid’s base lies the most critical element: adequate energy intake—ensuring you’re consuming enough calories to fuel your training. In this article, we dive deeper into why energy intake is essential and provide actionable tips to help you avoid the pitfalls of under-fueling.

Relative Energy Deficiency in Sport (REDs)

Let’s start with a brief history lesson. The Female Athlete Triad was first defined in 1977 by the American College of Sports Medicine as a syndrome found among female athletes and resulting from pressure to lose weight or maintain an unrealistically low body weight. Women with the triad tended to have eating disorders, amenorrhea (loss of menstrual period), and osteoporosis (bone disease) (Otis et al., 1997). This characterization was modified in 2007 to include low energy availability (LEA), menstrual dysfunction, and changes in bone mineral density (BMD) (Nattiv et al., 2007). With this change came the recognition that each component in the triad existed on a spectrum. For example, an athlete could suffer from the triad without a full-blown eating disorder or a diagnosis of osteoporosis.

Further research helped to improve understanding of the multifaceted consequences of LEA in athletes. Researchers came to realize that any athlete, regardless of sex or gender identity, could experience these consequences. Therefore, the characterization of the syndrome was once again modified and in 2014, the International Olympic Committee (IOC) introduced Relative Energy Deficiency in Sport (REDs) (Mountjoy et al., 2014).

Formally, REDs is defined as “a syndrome of impaired physiological and/or psychological functioning experienced by female and male athletes that is caused by exposure to problematic (prolonged and/or severe) low energy availability” (Mountjoy et al., 2023). In other words, REDs is a syndrome of possible negative health and performance outcomes resulting from a mismatch in energy intake and energy expenditure. Practically speaking, if your training volume increases but the amount that you eat does not, you are at risk of developing REDs.

Here are answers to some common questions about REDs:

• Is REDs the same thing as an eating disorder? While the LEA that causes REDs may result from an eating disorder, this is not always the case! Eating disorders and disordered eating are both strong risk factors for REDs, but there are many other causes of under-fueling in athletes. For example, particularly among endurance athletes with high training volumes, it can be practically challenging to meet calorie needs and relying on hunger cues alone can often result in under-fueling. If you’ve ever come back from a long run and the last thing you wanted to do was eat, you have experienced this firsthand. Because of this, having a healthy relationship with food does not necessarily mean that you are in the clear when it comes to REDs.
• What is the role of REDs in Overtraining Syndrome (OTS)? Overtraining Syndrome describes the physiological outcomes of a mismatch between training load and recovery (Meeusen et al., 2013). In a way, OTS and REDs are different ways of slicing the same pie since nutrition plays a major role in recovery. As such, there is a lot of overlap in symptoms resulting from OTS and REDs (Stellingwerff et al., 2021) and it is not uncommon for an athlete to experience both syndromes concurrently.
• Is REDs just a female problem? REDs can be experienced by any athlete, regardless of sex or gender identity. Research in men is limited, but there do seem to be differences in how REDs presents itself between men and women. Furthermore, it looks like most males can sustain a lower level of energy availability before symptoms result, compared with women (Mountjoy et al., 2023).

Consequences of REDs

Every athlete may experience different symptoms of REDs, depending on a number of factors, including the extent of LEA. The IOC developed a new set of conceptual models in 2023 to illustrate the potential consequences of REDs on health and performance. One model illustrates health consequences while the other illustrates performance consequences of REDs. LEA is located in the center of each model, representing its key role as a causal factor in REDs. Read on to learn more about these consequences.

Health Consequences

While the most well-documented health implications of REDs are reproductive (e.g., amenorrhea or loss of menstrual period in women, loss of libido in men) and bone dysfunction (e.g., stress fractures, osteoporosis), REDs can affect a plethora of body systems, as shown in the image below.

Importantly, LEA can affect physical as well as mental health, although the roles of depression, anxiety, and the development of eating disorders are still not clear (Mountjoy et al., 2023). There is likely a reciprocal relationship between mental health disorders and LEA, meaning that not eating enough can cause, for example, anxiety, while anxiety may also result in excess exercise or inadequate fueling.

Performance Consequences

While health consequences of REDs can lead to detrimental athletic performance (good luck training with a stress fracture or training through constant illness or poor sleep), there have also been some studies looking specifically at performance outcomes with REDs. These findings are shown in the figure below and include poor adaptation to training, decreased muscle strength, and decreased power and endurance.

Beyond Adequate Energy Intake

Adequate energy intake is a fancy way of saying “eating enough to meet your nutritional needs”. Can you avoid REDs by simply eating enough? While this may seem like the practical take away, the answer is actually more complicated thanks to two relatively new concepts:

1. Within-day energy deficiency. If you recall the Performance Pyramid, eating consistently throughout the day is of utmost importance for athletes. This is because of a concept called within-day energy balance. Overall energy balance is determined by subtracting the number of calories your body uses in a day from the number of calories you eat in a day. If you eat 3,000 calories but burn (through exercise and through your body’s regular functions) 3,500, you are in a 500 calorie deficit.

Within-day energy balance involves looking at energy intake and expenditure in one hour intervals throughout the day. Maybe between 8 and 9 AM, you eat 750 calories but burn 70. You are in a within-day energy surplus. But at 9 AM, you go for a run, burning 700 calories, while eating nothing. From 9-10 AM, you experience an energy deficit. Because your body is constantly using calories for its regular maintenance functions, any hour during which you don’t eat anything is an hour that you are experiencing an energy deficiency.

Research on this topic is still in its infancy, but it indicates that the more time spent in an energy deficiency, the more markers of REDs (including high cortisol and low testosterone levels) begin to appear (Torstveit et al., 2018). In one study, female athletes with menstrual dysfunction spent more hours with an energy deficiency compared to those with normal menstrual function (Fahrenholtz et al., 2018). 

2. Low carbohydrate availability (LCA). Pop quiz! Do you remember the important role that carbs play for athletes? Carbs are the muscles’ (and the brain’s) preferred source of energy – so without enough carbs, your athletic performance will suffer. And it turns out that not getting enough carbs can actually result in a set of very similar health and performance consequences as REDs. Indeed, LCA, even when overall intake is adequate, is related to poor bone health and immunity and reduced endurance and power (Lodge et al., 2023).

Diagnosis of REDs

Because research on REDs is still young, there are no standardized diagnostic criteria. To fill this gap, part of the IOC’s updated consensus statement in 2023 (Mountjoy et al., 2023) included a new clinical assessment tool to assist health care providers in identifying athletes at risk of REDs. This clinical assessment tool includes a number of indicators such as amenorrhea, low testosterone, history of bone stress injuries, high cholesterol, and symptoms of depression/anxiety, and categorizes athletes into risk groups. While this updated tool is likely to help standardize the diagnosis of REDs, more research is still needed to develop specific cut-points for each of these indicators. For now, diagnosis is up to the clinical judgment of your health care provider.

Treatment of REDs

Once you’re diagnosed with REDs, a team approach to treatment is recommended. Your treatment team should be individualized based on what issues you are experiencing, and may include sports medicine, nutrition, psychology, and physical therapy, among other medical specialties. Coaches should also be included in treatment conversations.

Indeed, the top priority in treatment is to increase energy availability through modifications to nutrition and training (Kiukman et al., 2021). Since REDs is caused by a mismatch between energy intake and output, bringing these variables into balance is key to recovery. This could involve eating more, training less, or a combination of the two.

Treatment of specific symptoms may also be indicated – although without correcting the root cause of REDs, this is only putting a Band-Aid on the problem. For example, if an athlete with REDs experiences gastrointestinal upset, treatment may include dietary modifications or medications to lessen GI distress. Similarly, depression may be treated through mental health therapy or possible medication.

Notably, although birth control pills are often prescribed to treat amenorrhea or other forms of menstrual dysfunction, monthly bleeding does not indicate improvement in REDs! This is because the “period” that you get while taking hormonal birth control is not actually a menstrual period – it is called withdrawal bleeding and occurs as a response to the week-long break in hormones while taking placebo pills. Withdrawal bleeding will occur even if your energy availability and resulting hormonal function has not improved.

Prevention of REDs and the Role of Weight in Performance 

The best form of treatment is simply matching your intake to your output. In other words, by eating enough to account for your training volume, you can reduce your risk of REDs.

This is easier said than done, especially for athletes involved in sports like climbing and running, where being thin, “looking like an athlete”, and having less weight to carry uphill is praised. As uphill athletes, we all have a responsibility to push back against this culture and set a good example for our peers.

In fact, weight may not play as much of a role in sports like climbing as commonly believed. Research on the relationship between weight and climbing performance presents mixed results (Ginszt et al., 2023), with many studies finding no significant relationship between measures like BMI or body fat percentage and climbing performance (Gudmund, 2019; Saul et al., 2019). One study found that body fat percentage, but not body mass index (BMI), was significantly different between elite and advanced climbers (Giles et al., 2020), which may indicate that a common fear of building muscle may not be well-founded.

The role of weight has also been studied substantially in runners. In a classic 1978 study, runners’ paces were measured over a 12-minute run while wearing different sized weight vests (Cureton et al., 1978). The results? For every additional pound, runners were approximately 1.5 seconds per mile slower. This is unlikely to make a difference for uphill athletes – even those competing at the highest levels. Studies of road and track runners (Alvero-Cruz et al., 2020) and trail runners (Alvero-Cruz et al., 2019) have found significant associations between measures of weight, such as BMI, and race performance. However, in most cases, weight was a weaker predictor of performance than metrics like weekly training load, years of running experience, and VO2 max. What does this tell us? People who run more tend to be stronger runners and also tend to weigh less. Importantly: this does not tell us that losing weight is the secret sauce to all of your performance challenges.

Furthermore, disordered eating and rates of under-fueling are high in both climbers (Joubert et al., 2020; Monedero et al., 2023) and runners (Dambacher et al., 2023; Dervish et al., 2022; Jesus et al., 2021; Lane et al., 2019). Rather than a lower BMI improving performance, perhaps high performers tend to have a lower BMI due to their disordered eating. In other words, athletes who train hard for many years (and who may be gifted genetically) tend to perform well – and also weigh less.

Ultimately, while weight loss may improve your performance in the short term, it is limited in its effect. No matter how much you weigh, you will eventually reach a point where you no longer have weight to lose (and this point often happens sooner than expected). Then what will you do to progress? Rather than buying into the “lighter is better” mindset, what can you do to improve your performance? Base building, strength training, and – you guessed it – eating enough can help you progress in sport in a more sustainable way than losing a few pounds or trying to maintain a weight that is not right for your body.

How to Make Sure You’re Eating Enough

For so many reasons, the answer to this question is tricky. Countless calculators exist online to estimate your energy needs, but these are merely estimates based on the average person and can be highly inaccurate (O’Neill et al., 2023). Add in the uncertainty of mountain sports and you have an even less accurate estimate as it can be difficult to assess calorie burn when the terrain is steep or technical or you are climbing at high altitudes. Wearables like smart watches offer a promising alternative, especially when combined with a heart rate monitor, but even they shouldn’t be relied upon (O’Driscoll et al., 2020).

Weight loss is a good indicator that you are not meeting your needs – but don’t put all your eggs in the weight basket! Just because you are maintaining your weight does not mean that you are eating enough. Your body wants to preserve mass. If you’ve ever reached a “plateau” in a weight loss effort, you’ve experienced this. In order to do so, your body will slow down other processes to conserve energy while sparing body fat. This can include apparent changes like reduced heart rate and thermogenesis (your body’s heat-producing mechanism) but can also include changes that aren’t as obvious until they become a problem – like reduced bone mineral density, which is unfortunately too often discovered after the diagnosis of a stress fracture or osteoporosis.

 Here are some practical tips to ensure that you are meeting your needs:

• Eat when you’re hungry. Whether your stomach is growling or you’re starting to feel sluggish and irritable, if you’re hungry, your body is letting you know that it needs food. It may not always be practical to eat when hunger hits but try not to make a habit of ignoring these signs.
• Eat when you’re not hungry. As an athlete, there will probably be times that you will need to eat when you’re not hungry – such as after a hard workout. If you limit yourself to only eating when you feel physical hunger, not only will you be missing out on critical recovery windows, you also risk being under-fueled.
• Eat regularly. A good starting point for uphill athletes is to avoid going more than three or four hours without eating while awake. For most people, this will look like three meals and two or three snacks each day.
• Don’t dig yourself too deep of a hole. During a long day in the mountains, it is almost impossible to eat enough to match the calories you are burning. Even if your stomach could tolerate taking in enough calories, your body wouldn’t be able to process and utilize this energy. Despite this, you can minimize the hole that you dig yourself into by eating what you can while on the go. The more you eat while you’re running or climbing, the less you have to make up for afterwards.
• Don’t train fasted. Fasted training is a hot topic, with proponents pointing toward improvements in performance. However, research does not overwhelmingly support this claim (Aird et al., 2018; Correia et al., 2020) and, furthermore, fasted training has a dark side that may include inadequate calorie intake and increased risk of injury (Scott et al., 2012; Williamson & Moore, 2021). Additionally, training fasted increases time spent in a within-day energy deficiency, which contributes to bone and hormonal dysfunction.
• Think liquid. If you find it hard to chew your food when you’re not hungry, you may want to incorporate liquid sources of nutrition, like smoothies, juice, and sports drinks, in between meals as easy-to-get-down bonus calories.
• Monitor data such as weight and menstrual period. Even though a stable weight and a regular period don’t mean that you’re in the clear, weight loss or changes to your cycle may indicate that you’re not eating enough. Take corrective action if you see a change in either metric.

What To Do If You Think You Have REDs

If anything you’ve read today raises a red flag, talk to your doctor. In addition, because the symptoms of REDs will not resolve until your nutritional intake matches your training output, don’t hesitate to reach out to a Registered Dietitian, like through Nutrition Coaching here at Uphill Athlete. Nutrition Coaching can not only help you to determine the appropriate amount of food for your body and your training volume but can also help you to work through any challenges that you face in your relationship with food.

As a bonus, if you are coached through Uphill Athlete, you will receive a team approach in which your dietitian and your coach are in close communication, making the correct modifications to your training plan to ensure a speedy recovery and to reduce your risk of injury.

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