Gut feeling: keeping the tummy blues at bay

Gastric distress can ruin even the best-laid race plans, and make life generally miserable for endurance athletes in training. Andrew Hamilton looks at the causes of this potentially debilitating condition, and what the science says about how to successfully overcome it

On a cold January morning many moons ago, I had an unforgettable training run – but for all the wrong reasons. Having set off for a 12-miler, I was afflicted with severe tummy cramps just four miles into the run, despite running on an empty tummy. The pain became progressively worse, as was the urge to use the toilet. Luckily, my route consisted of two laps, which meant passing my house halfway round, and I was able to limp home – just! What I had experienced was a bad case of ‘gastric distress’, no doubt exacerbated by the large amount of apricots I had eaten the previous day.

What is gastric distress?

My episode of gastric distress was particularly memorable because it was an unusual occurrence. For many athletes unfortunately, gastric distress is an all-too-regular occurrence, and something that can blight training and race performance. The symptoms of gastric distress in athletes - more correctly known as exercise-induced gastrointestinal (GI) distress – can vary in type, intensity and frequency. However the most typical manifestations include:

• Diarrhoea
• Cramping in the gut
• Nausea
• Gastric pain

Typically, more than one symptom will occur in GI distress.

If you suffer regularly from GI distress, you’re not alone. GI distress is frequently reported by endurance athletes in long-distance events such as marathons^{Sports Med 1988. 26:365–37}. Indeed, it has been estimated that 30 to 65% of long-distance runners are prone to experiencing some GI-distress symptoms related to exercise including nausea, vomiting, abdominal cramps and the urge to have a bowel movement^{Br. J Sports Med 1988. 22:71–74}.

A more recent study pooled the findings from other studies and found that the prevalence of GI symptoms during exercise varied from 30% up to as high as 90%^{Sports Med 2014. 44 (Suppl 1):S79–S85}!

In addition to the high prevalence of these symptoms, exercise-induced GI distress can and often does harm athletic performance and in some cases, lead to dropping out of the competition^{Int J Sports Physiol Perform 2011. 6:25–37}. This phenomenon is nothing new either. The marathon legend Bill Rodgers (figure 1), with four victories in both the Boston marathon and the New York City marathon in the late 1970s, once said: “More marathons are won or lost in the porta-toilets than at the dinner table.” This illustrates the magnitude of the problem for endurance athletes, particularly long-distance runners.

Figure 1: Bill Rodgers

What causes GI distress?

To understand how athletes can overcome GI distress, it helps to understand what causes it. Unfortunately, the exact physiological mechanisms that lead to GI distress are not fully understood. It’s also a mystery as to why some athletes remain asymptomatic despite showing some of the physiological changes that produces symptoms in other athletes.

On a broad-brush scale, we know that GI distress is most likely to arise when a combination of factors comes together: physiological, mechanical and nutritional (see figure 2):

• Physiological - exercise results in numerous physical and chemical changes in the intestinal tract, and most of these effects are intensity dependent. Many of the functions are not affected at low-intensity exercise but become progressively affected at higher intensities. Without doubt, one of the main culprits behind GI symptoms during exercise is splanchnic hypoperfusion (see box 1^{Aliment Pharmacol Ther 2012. 35:516–528 Am J Physiol Gastrointest Liver Physiol 2012. 303:G155–G16}). Splanchnic hypoperfusion during exercise can lead to intestinal ischemia (lack of oxygen), which subsequently damages intestinal epithelial cells and compromises the intestinal barrier function (ie makes the gut more ‘leaky’). The evidence for this ‘leaky gut’ effect is strong as multiple studies have demonstrated clearly that (particularly intense) exercise increases in intestinal permeability^{Scand J Gastroenterol 1992. 27:270–274 Am J Physiol Gastrointest Liver Physiol 2011. 300:G477–G484 Med Sci Sports Exerc 2012. 44:2257–2262 Am J Clin Nutr 2016. 104:526–53}.

• Mechanical - mechanical causes of gastrointestinal problems are related to either impact or posture. We know for example that GI distress is more common in runners than in cyclists^{Int J Sports Med. 2000;21:65–7}, which is most likely a result of the repetitive high-impact mechanics of running and subsequent damage to the intestinal lining^{Aust J Sci Med Sport. 1995;27:3–8}. This repetitive gastric jostling is also thought to contribute to lower-gastrointestinal symptoms such as flatulence, diarrhoea, and urgency. However, posture can also have an effect on gastrointestinal symptoms. For example, upper gastrointestinal symptoms are more prevalent on a bike - possibly due to increased pressure on the abdomen as a result of the cycling position, particularly when in the ‘aero’ position.

• Nutritional - It has long been known that nutrition can have a strong influence on gastrointestinal distress. In particular, foods high in fibre, fat, protein, and the fruit sugar fructose have all been associated with a greater risk of developing gastrointestinal symptoms. Studies on triathletes have also shown that the use of more concentrated carbohydrate drinks (a concentration greater than 500 milliosmoles per litre) was more likely to result in symptoms of GI distress. Importantly however, many of the problems can seem to be diet related but occur in the absence of any food or drink intake before or during exercise. One possible explanation is the some foods consumed regularly in the diet can cause problems in the lower intestine via a process of bacterial fermentation. New research suggests that reducing these foods (dubbed ‘FODMAPs’) in the diet can help reduce the risk of GI distress – something that we’ll look at shortly.

Figure 2: Mechanical, physiological and nutritional factors in GI distress

Understanding terminology: What is splanchnic hypoperfusion?

Splanchnic hypoperfusion is a condition where the normal patterns of blood flow to the intestines and organs in the abdominal region are disturbed for example during vigorous exercise, when blood is directed away from the abdominal region to supply the working muscles with more blood (and oxygen).

When SH occurs, the result is micro-trauma/injury to the small intestine, which then causes the gut to become ‘leaky’. This in turn results in a range of gastrointestinal symptoms such as cramps and nausea, which can severely dent athletic performance. The good news is that recent research suggests citrulline can help preserve blood flow to the small intestine, which could help reduce the incidence of SH in athletes (more on this later).

Strategies to reduce GI distress

As we said at the outset, our scientific understanding of the causes of GI distress is still in its infancy, and more research is needed. However, we do know enough to be able to confidently reduce the risk of GI distress with some targeted strategies. These strategies are aimed at reducing the physiological, mechanical and nutritional loading on the gut, which cumulatively can make a big difference in how you feel and perform! With that in mind, let’s take each element in turn.

Physiological strategies

Strategies here involve reducing splanchnic hypoperfusion and/or intestinal permeability. Because this involves changes in gut physiology, it might not surprise you to learn that these strategies focus on nutrients taken orally.

*Citrulline – Citrulline is a naturally occurring amino acid. Unlike many amino acids however, citrulline is not used to build structural proteins in the body. It’s also a ‘non-essential’ amino acid, which means that when conditions are right, the body can make it from other compounds. Citrulline is found naturally in some foods and one of the very best sources is watermelon. Indeed, the name ‘citrulline’ is actually derived from from citrullus, the Latin word for watermelon!

Although much of the research on citrulline has centred on enhancing actual exercise performance, a fascinating study suggests that citrulline could help reduce gastric distress during exercise but preventing splanchnic hypoperfusion^{Med Sci Sports Exerc. 2014 Nov;46(11):2039-46}. In a randomised, double-blinded crossover study (the most scientifically rigorous of the lot), ten men cycled for 60 minutes on two separate occasions at 70% of their maximum workload (moderately hard) after taking 10 grams of L-citrulline (10 g) or an inert placebo. During both trials, the blood flow to the gut was assessed and the levels of amino acids circulating in the bloodstream were measured every ten minutes.

When the subjects took the citrulline, the blood flow to the gut was unaltered during exercise (ie SH was prevented) and there was no indication of increased damage to the intestine. When they took the placebo however, the phenomenon of splanchnic hypoperfusion was observed in the subjects and this was also accompanied by increased markers of intestinal damage. How did the citrulline exert its protective effect? The most likely explanation is that when converted to arginine in gut region, the production of nitric oxide was increased, and since nitric oxide increases blood flow in small blood vessels, this helped to offset any tendency towards SH (see figure 3).

Figure 3: A simplified diagram showing the relationship between citrulline, arginine and nitric oxide



Citrulline is readily converted in the body to another amino acid called arginine. That’s important because arginine can readily be used to make a key signalling molecule called nitric oxide, which has the ability to increase blood flow through muscles and other tissues – in this case helping to reduce the risk of splanchnic hypoperfusion.

*Bovine colostrum – Some research suggests that bovine colostrum supplementation could help combat gastric distress. The logic is thus: the gut is responsible for nutrient absorption, detoxification and supporting immune function. The major player here is a special immunoglobulin protein called secretory IgA (sIgA); individuals with chronic gut problems, such as irritable bowel syndrome Crohn's disease, ulcerative colitis etc typically have low levels of sIgA. Colostrum contains very high levels of sIgA; researchers have theorised that supplementing with boving colostrum could top up slgA, reduce inflammatory and pathogenic species in the gut, and help heal intestinal problems such as leaky gut syndrome and other permeability problems.

A 2011 study by British researchers, found compelling evidence for the potential benefits of consuming bovine colostrum^{Am J Physiol Gastrointest Liver Physiol 2011. 300:G477–G484}. In a double-blind, placebo-controlled, crossover study (the most rigorous kind of scientific study), twelve volunteers (runners and rugby players) completed a standardised exercise challenge, consisting of running uphill on a treadmill at 80% of VO2max (hard) for 20 minutes.

For 14 days before the exercise challenge, the subjects took either 20 grams per day of bovine colostrum or an inert placebo – but one that provided the same number of calories and overall levels of protein/carbohydrate. Immediately after the exercise trial, measures of gut permeability were taken from all the subjects. After a two-week ‘washout’ period, the whole procedure was repeated but this time reversed (crossover) - ie those who had taken the placebo now took colostrum and vice versa. The key finding was that when the subjects took the placebo, their gut permeability increased 2.5-fold. However, when they had been consuming colostrum, this rise was in permeability was reduced by 80% (see figure 4).

Figure 4: Gut permeability following intense exercise ^{Am J Physiol Gastrointest Liver Physiol 2011. 300:G477–G484}

Each line corresponds to a different subject. The higher the ratio (left axis), the higher the gut permeability. When subjects took colostrum (shown right), the rise in permeability was minimal.

*Glutamine – Glutamine is another amino acid, which – in sports science at least - has traditionally been researched for its potential as a recovery nutrient. However, some recent research suggests that glutamine could also help reduce the risk of GI distress by reducing intestinal permeability during exercise. In a 2017 study, ten recreationally active males completed a total of four exercise trials during which they ran at 70% of VO2max (moderate hard) for 60 minutes on a treadmill in hot (30C) conditions (exercising in heat is known to increase the likelihood of GI distress)(14). However, two hours before exercise the runners consumed different drinks. These contained as follows:

· 0.25 grams of glutamine per kilo of bodyweight

· 0.50 grams of glutamine per kilo of bodyweight

· 0.9 grams of glutamine per kilo of bodyweight

· No glutamine (control trial)

During and after the trials, blood tests were carried out to assess how ‘leaky’ the runners’ intestines had become, and it was clear that all three doses of glutamine reduced the level of leakiness compared to the control condition. The authors went onto conclude that 'athletes competing in the heat may benefit from acute glutamine supplementation prior to exercise in order to maintain gastrointestinal integrity’.

Nutritional strategies

The goal here is to adjust the diet to reduce or remove foods that are known to help precipitate GI distress in an individual. Note however that this is highly individual – there is no ‘one size fits all’ strategy. In plain English, just because a certain dietary strategy works for your mate, it doesn’t mean it’ll work for you!

*Day-to-day diet: the ‘FODMAP’ approach – What the hell is FODMAP I hear you ask? This acronym actually stands for:

Fermentable Oligosaccharides, Disaccharides MonosAccharides and Polyols.

All of these are types of natural sugars and therefore all carbohydrates. Examples of these carbohydrates include:

• Fermentable oligosaccharides - fructans and galacto-oligosaccharides
• Disaccharides - lactose
• Monosaccharides - excess fructose
• Polyols - sorbitol, mannitol, maltitol, xylitol and isomalt

FODMAPs are found in a wide range of foods (see table 1). The key point is that these carbohydrate sugars tend to be poorly absorbed and pass through the small intestine and enter the colon, where they are fermented by bacteria. Gas is then produced, which stretches the sensitive bowel causing bloating, wind and pain. This can also cause water to move into and out of the colon, causing diarrhoea, constipation or a combination of both. The FODMAP approach is quite new. Importantly however, its use has recently been validated in athletes who suffer from GI distress during exercise using properly controlled scientific trials^{Med Sci Sports Exerc. 2018 Jan;50(1):116-123}.

TABLE 1 EXAMPLES OF FODMAP FOODS 2022 10 04

		FODMAP TYPE	#colspan#
Fructans	Galacto-oligosaccharides	Lactose	Excess fructose	Polyols
Wheat	Baked beans	Animal milks	Apples	Nectarines
Rye	Lentils	Custard	Pears	Peaches
Barley	Borlotti beans	Ice cream	Mangoes	Plums
Garlic	Chickpeas	Condensed milk	Watermelon	Cauliflower
Leek	Soybeans	Evaporated milk	High-fructose corn syrup	Apricots
Onion	Kidney beans	Yogurt	Honey	Mushrooms
Lentils		Dairy desserts		Sugar Snaps
Chickpeas		Rye		Chewing gum
Legumes		Barley		Confectionery with polyols
Cashews
Pistachios

In the FODMAP approach, high FODMAP foods are eliminated from the diet for six to eight weeks and replaced with suitable alternatives (see figure 5). This is best done in consultation with a dietician who can guide you to ensure your diet remains nutritionally adequate.

After this, small amounts of FODMAP foods are gradually re-introduced (one at a time) to find a level of tolerance without the symptoms returning. It is important to remember however that not everyone will have a problem with every FODMAP. Some people might have symptoms triggered by just one or two types of FODMAPs, whereas others may be sensitive to all five. The reasons for this are unknown, but foods should only be restricted if they contribute to symptoms. The diet needs be individualised according to the problematic FODMAP. The end result should be a long-term diet that is lower in the problematic FODMAPs than were originally consumed, but is not as FODMAP-restricted as the first phase of the diet. You also need to bear in mind that high-FODMAP foods are important for stimulating the growth of beneficial bacteria in the gut, so simply eliminating all of them for long periods of time is not recommended for long-term gut health.

Figure 5: FODMAP foods and suitable alternatives

*Energy drinks during exercise - For athletes who compete in endurance events, an interesting observation is that when a carbohydrate beverage is consumed that contains multiple transportable carbohydrates such as glucose and fructose, gastrointestinal symptoms seem to be reduced compared with the consumption of the same (large) amount of a single carbohydrate (glucose). This has been a consistent finding in a number of studies^{J Appl Physiol. 2006;100:807–816 J Appl Physiol. 2006;100:1134–114 Med Sci Sports Exerc. 2004;36:1551–1558 J Appl Physiol. 2004;96:1285–1291}.

This might seem at odds with the FODMAP approach above, where excess fructose in the diet can increase GI distress. However, if you don’t suffer from GI distress when taking no carbs DURING exercise, but taking carbohydrate products during exercise produces distress, then using a glucose-fructose drink may provide a solution (no pun intended). That’s because it suggests the problem is less about gut fermentation and more about the ingested carbohydrate during exercise not being absorbed rapidly enough. By providing two routes of absorption rather than just one, a glucose-fructose drink can help overcome this problem, especially for athletes consuming carbohydrate at high intake levels (over 60 grams per hour).

Box 2: Non-steroidal anti-inflammatory drugs (NSAIDs)

Large numbers of athletes have reported that they use using analgesics to relieve existing or anticipated pain. But that could be a problem because the use of NSAIDs has been associated with a three-to fivefold increased risk of upper gastrointestinal complications, mucosal bleeding, or perforation compared with no medication^{Ann Intern Med. 1991;115:787–796}. In a study at the Chicago marathon, it was found that ibuprofen (but not aspirin) ingestion during prolonged exercise may have increased gastrointestinal permeability in runners and led to gastrointestinal symptoms^{Int J Sport Nutr. 1999;9:426–43}. Scientists have also demonstrated that ibuprofen aggravates exercise-induced small intestinal injury and induces gut barrier dysfunction, and concluded that the consumption of NSAIDs by athletes is not harmless and should be discouraged in those who experience persistent or recurring gastrointestinal symptoms^{Med Sci Sports Exerc. 2012;44:2257–2262}.

Mechanical strategies

Eliminating the movement patterns associated with your sport just isn’t possible. No amount of attention to running form will prevent the up and down oscillation that characterises the running action. Likewise, if you need to get down low on the handles for an aero cycling position, there’s no way round it. The good news however is that some research suggests you can, to a limited extent, ‘train your gut’ to be less sensitive to GI distress resulting from consuming carbohydrate during exercise^{Curr Sports Med Rep. 2006;5:161–164}.

In one study, researchers showed that athletes who are not accustomed to fluid and food ingestion during exercise had a twofold risk of developing gastrointestinal symptoms than athletes who were accustomed to taking fluid and food during exercise^{Scand J Gastroenterol. 2008;43:1477–148}. In another, 16 endurance-trained cyclists and triathletes were pair matched and randomly allocated to either a high carbohydrate group or an energy-matched low carbohydrate group for 28 days^{J Appl Physiol. 2010;109:126–13}. After 28 days, the high-carbohydrate group were shown to have superior rates of carbohydrate absorption, which is associated with improved tolerance of fluids and foods during exercise, and consequently, reduced the chances of GI distress. Moreover, studies have also shown that repeated sessions of drinking while running lessens the feeling of stomach discomfort, even though the rate stomach emptying doesn’t change^{Int J Sports Med. 2008;29:878–88}.

In practice, what this means is that if you make a point of regularly ingesting carbohydrate foods or fluids in training, your tummy is likely to become more tolerant. This also serves to underline the point that in a race situation, you should only ever use feeding strategies that have been repeatedly tried and tested in training. Saving a new strategy for race day or the impulsive use of sports drinks and snacks is likely at best to result in discomfort or at worst, completely scupper your performance. It’s also important to point out however, that this ‘training the gut’ strategy is NOT effective for those who suffer from GI distress even on an empty stomach. If you’re such an individual, you’ll need to look at your day-to-day diet with the FODMAP approach, and also consider using nutrients to reduce splanchnic hypoperfusion/gut permeability.

Practical summary

There are a number of practical recommendations in this article, but for convenience, we will summarise them here:

If you suffer from gastric distress only when consuming drinks and food on the move:

• Switch to glucose-fructose carbohydrate drinks.
• Make sure your drinks aren’t too concentrated (keep them below 60 grams of carbs per litre).
• Try spreading out your intake more evenly – ie lots of little sips/bites rather than taking on board a large quantity occasionally.
• Practice feeding strategies in training – you might find that your tolerance increases over time.
• Avoid using anti-inflammatory medications such as Ibuprofen unless you absolutely need them.
• Make sure your pre-training meal is reasonably low in fat and not too fibre rich. Consume it at least two hours before training.
• Consider the use of supplements such as citrulline, glutamine and bovine colostrum to minimise gastric distress. Research suggests that 5-10 grams of citrulline can reduce GI distress. If you do experiment, try only one supplement at a time so that you ca