When athletes think of their training programs, they often think of preparing their lungs, their hearts, and their muscles to withstand the rigors of vigorous exercise. Few athletes take into consideration that the gut, the gastrointestinal (GI) system, also must cope with and adapt to the demands of heavy training. Fortunately, the gut has the capacity to adjust to the demands of training, adaptations that are mostly transparent because they occur naturally in response to improved fitness and increased daily energy intake. Provided the athlete drinks sufficiently during training and competition to avoid hypovolemia, hyperthermia, and hypoglycemia, the human gut is well designed to meet the demands of even the most vigorous exercise.
Although the gut has an enormous capacity for water and nutrient absorption during rest and exercise, GI complaints among athletes are quite common. Most such complaints are typically mild, usually transient, present little risk to health, yet can be bothersome and have the potential to impair performance. Other GI complaints can reflect severe and life-threatening disorders, as evidenced by athletes who have suffered from ischemic colitis brought on by the combination of physical exhaustion, hyperthermia, and hypovolemia [1••,2]. Accumulating evidence leaves little doubt that competing in prolonged exercise such as marathons, ultramarathons, and Ironman-distance triathlons can result in pathophysiologic changes such as gastric and intestinal lesions and increased intestinal permeability . The gut can not adapt to such severe insults and under these circumstances, even the fittest, most acclimated athletes remain at risk of significant GI injury.
Consider, for example, the case of Derek Clayton, the great Australian marathoner who experienced debilitating GI problems after setting a world record of 2:08:33 in 1969 (a mark that stood for 12 years). Two hours after the race, Clayton began urinating blood clots, vomiting black mucous, and defecating voluminous black diarrhea, symptoms that remained for the next 48 hours . Clayton's GI problems were certainly extreme and his world record all the more astonishing because just 11 days beforehand he had run a 2:17:26 marathon in the heat of Ankara, Turkey. Clayton noted subsequently that he never took a drink at any aid station during his best marathon races, so it is likely that his GI symptoms in 1969 were due to ischemic bowel injury caused by a severe reduction in splanchnic blood flow in response to the hypovolemia (and possible short-term hyperthermia) associated with his world-record effort.
GI Physiology During Exercise
The current scientific consensus is that the majority of GI complaints during exercise occur because of reduced gastric emptying, malabsorption of water and nutrients, delayed transit time, or a reduction in splanchnic blood flow, all of which can give rise to GI symptoms such as abdominal cramps, acid reflux, heartburn, bloating, side-ache (side-stitch), persistent eructation and flatulence, nausea, vomiting, urge to defecate, loose stool, bloody stool, and diarrhea.
Gastric emptying rate is impeded by high-intensity exercise (> 70% VO2max) and further slowed by dehydration and hyperthermia, so reduced gastric emptying alone could be responsible for upper-GI complaints such as nausea, vomiting, eructation, reflux, heartburn, side-ache, and chest pain. Gastric emptying rate is most sensitive to the energy content in the stomach, so it is not surprising that high-energy (> 7% carbohydrate), hypertonic drinks give rise to greater GI complaints . Side-ache appears to be linked to physical “tugging” on the viscera , as can occur with the sloshing and fullness often associated with delayed gastric emptying. GI reflux, a symptom that can also be related to delayed gastric emptying, is greater in running , is increased by pre-exercise food intake, and may be related to inadequate lower esophageal sphincter pressure [8••].
There is little evidence that the absorptive capacity of the small intestine is impaired during exercise because even though exercise causes a substantial fall in gut blood flow, the length of the small intestine more than compensates for any local reduction in water or solute absorption . There is evidence that orocecal transit time is altered by exercise (delayed in some studies, accelerated in others) and that the urge to defecate following exercise may be due to a decrease in colonic motility during exercise (offering less resistance to colonic flow), coupled with an increase in propulsive activity after exercise . During exercise, sympathetic stimulation reduces gut blood flow but also relaxes gut tone, and this may increase the passage of colonic contents into the rectum, a response that may be further promoted by the up and down nature of running. Distension of the colon may affect GI function upstream because colonic distension may provide feedback inhibition to reduce gastric emptying rate, prolonging orocecal transit time. Athletes who consume a vegetarian diet or athletes who ingest a high-fiber meal or snack prior to exercise are more prone to GI problems because dietary fiber increases intestinal bulk and water content . Athletes prone to GI disturbances have longer oraocecal transit times and may be more prone to altered intestinal permeability [12•].
The mental stress of competition, vigorous exercise, hyperthermia, hypovolemia, hypoglycemia, and exhaustion all increase sympathetic discharge and can reduce splanchnic blood flow by 50% to 80%, so it is not surprising that reduced gut blood flow during prolonged exercise might cause GI problems. Splanchnic blood flow (in the celiac and mesenteric arteries) decreases in proportion to exercise intensity and in response to dehydration, helping preserve central blood volume and pressure . Simply put, the higher the heart rate, the lower the splanchnic blood flow.
The reduction in splanchnic blood flow is usually tolerated without issue because the gut can withstand roughly 12 hours of a 75% reduction in blood flow at rest without any noticeable histologic effects . However, the ischemia, hypoxia, and hyperthermia that can occur during exercise can cause portions of the intestine to lose functional integrity, causing tissue lesions, necrosis, and increased membrane permeability.
In the small intestine, the tips of the microvilli normally have low PO2 because of the countercurrent exchange configuration between the arteries and veins and/or because of higher metabolic activity at the villus tip. Whatever the reason, microvilli are susceptible to prolonged vasoconstriction and permeability of the intestinal epithelial membrane increases with insufficient perfusion . Increased permeability allows entry of lipopolysaccharides and the initiation of immunologic and inflammatory events that can further alter gut structure and function and impair the athlete's thermal tolerance [8••].
Even otherwise healthy endurance athletes can experience bouts of bloody stool that can be due to hemorrhagic gastritis or transient intestinal ischemia [1••]. As Eichner  pointed out, it is important to determine if GI bleeding is “occult and trivial or overt and grave.” Even occasionally bloody stool can be a problem for athletes, particularly female athletes, because it can predispose to anemia. Persistently bloody stool, especially when coupled with abdominal pain and diarrhea, can indicate ischemic bowel disease.
GI Adaptations to Training
What is the evidence that the gut is capable of adapting to the increasing demands of training, akin to the adaptations in muscular, cardiovascular, and thermoregulatory responses? Does the gut increase its capacity to handle the large amounts of water and nutrients needed to sustain prolonged exercise, especially in the heat?
There is little doubt that the stomach can be “trained” to accommodate increasing volumes of food and drink. The volume of an empty stomach is 50 to 100 mL, but can increase quickly to roughly 1 L without an increase in intragastric pressure . World records for speed eating indicate that at least some human stomachs are capable of expanding well beyond 1 L. For example, in 2004, 131-lb Takeru Kobayashi consumed 53.5 hotdogs in 12 minutes. In the same year, Sonya Thomas, a 105-lb American, ate 11 lbs of cheesecake in 9 minutes .
In addition to the stomach's ability to expand to accommodate large volumes of food and drink, there is some evidence that gastric emptying rate may be enhanced with training [8••]. One possible explanation for that change is that a “learning effect” occurs as athletes become more accustomed to training with fluid in their stomachs [17•]. Interestingly, both gastric emptying rate and orocecal transit time have been reported to be enhanced in endurance athletes [18,19], possible adaptive responses to the large energy intake required during the day and to the repeated experience of ingesting food and drink during exercise.
Gisolfi [8••] noted that there is evidence of hyperphagia in the small intestine of some animal species in response to increased energy intake and reasoned that the same might be true for athletes. Regardless, the human small intestine has an enormous capacity for water and nutrient absorption even in nonathletes , so if hyperphagia of intestinal villi does occur in athletes, it may serve to minimize the risk of osmotic dumping after large meals, rather than provide an advantage during training and competition.
Splanchnic blood flow is greater in trained subjects at any given workload and there is evidence of improved gut barrier function with training because of greater splanchnic blood flow; whether local changes in the gut epithelium occur to provide further barrier protection remains to be determined. The loose stool frequently observed early in training or during abrupt increases in training load, typically resolves as training progresses, an adaptation that may result from greater splanchnic perfusion [8••].
In summary, the scientific literature provides what might best be termed “tidbits of evidence” indicating that the gut adapts to training. Additional research is required to confirm the breadth, magnitude, and meaning of such adaptations. However, there is little doubt that some adaptations occur during training that allow athletes to ingest impressive quantities of water and nutrients, usually without issue. For example, consider an Ironman triathlete who, during a 12-hour race, might ingest in excess of 10 L of fluid, 3000 calories from carbohydrate alone, and 5 tsp of salt. During periods of heavy training, it is not unusual for some athletes to ingest 5000 to 6000 kcal per day, along with 6 to 8 L or more of fluid.
In 1993, Brouns and Beckers [20•] published an excellent review article on gut function during exercise that included a list of practical recommendations to prepare the gut for competition. Their recommendations are, with slight modification, still applicable today:
- Get fit and acclimatized: thermal tolerance, splanchnic blood flow, and the integrity of the intestinal membrane all improve with training and acclimation to the heat.
- Stay hydrated: drinking during exercise to minimize body weight loss is the most effective way to avoid hypovolemia and hyperthermia. In addition, ingesting sufficient water and nutrients during prolonged exercise can help maintain splanchnic blood flow and reduce the risk of GI disturbances. Hypovolemia increases the frequency of GI complaints; 80% of marathoners who lost over 4% body weight complained of GI symptoms .
- Practice drinking during training: the capacity to comfortably ingest water and nutrients can be improved with training. Athletes should be encouraged to practice in their training sessions the fluid intake regimen they expect to follow in competition.
- Avoid over-nutrition before and during exercise: our anecdotal observations from a variety of laboratory experiments, along with as-yet unpublished survey data we collected at the 2005 Coeur d'Alene and Kona triathlon races, biases us to the conclusion that the GI discomfort reported by many athletes is associated with inappropriately large energy intake during exercise, often coupled with dehydration, and likely exacerbated by the normal changes in gut blood flow and motility that accompany exercise. Brouns et al.  reached a similar conclusion in 1987. Many athletes do not recognize that there is a limit to the body's capacity to oxidize exogenous fuel during exercise  and they often exceed that limit (roughly 60 g of carbohydrate per hour; ∼ 250 kcal/h), an error that predisposes them to slower gastric emptying, impaired water and nutrient absorption, and an increase in common GI symptoms such as bloating, belching, nausea, and diarrhea.
- Avoid high-energy, hypertonic foods and drinks before (within 30–60 min) and during exercise: it is important to maximize gastric emptying during exercise, particularly during exercise in the heat when replacing sweat loss is critical. When large sweat losses are expected, ingesting water or a properly formulated sports drink 15 to 30 min before exercise will assure that gastric emptying is not impeded. It is also helpful to limit fat and protein intake before exercise for the same reasons.
- Ingest a high-energy, high-carbohydrate diet: the gut adapts its capacity for nutrient absorption based on the nutrient content of the diet . A high-energy, high-carbohydrate diet might help decrease the risk of GI problems during exercise, certainly maximizes muscle glycogen stores, and reduces the risk of hypoglycemia.
- Avoid high-fiber foods before exercise: fiber attracts water into the gut, increasing the likelihood of GI discomfort.
- If prone to GI problems, limit nonsteroidal anti-inflammatory drugs (especially ibuprofen ), alcohol, caffeine, antibiotics, and nutritional supplements before and during exercise. Athletes should experiment during training to identify, and eliminate, factors that trigger gut sensitivity.
- Urinate and defecate prior to exercise: for obvious reasons, it pays to begin prolonged, vigorous exercise with an empty (or near-empty) bladder and colon. When significant sweat loss is anticipated, it is helpful to begin exercise with a stomach comfortably full of fluid to help maximize gastric emptying rate and achieve a head start on replacing sweat losses.
- Consult a physician if GI problems persist, particularly abdominal pain, diarrhea, or bloody stool: these are symptoms of ischemic bowel disease and warrant the attention of a physician, as do any recurrent GI problems that accompany exercise.
There is scientific evidence to suggest the gut can adapt to physical training in ways that improve its capacity for processing the large amounts of food and fluid required by athletes, reduce the risk of GI discomfort, and protect against gut-related injury during vigorous exercise. That said, there remains a lot to be learned about the extent to which training-related adaptations occur in the GI system.
There is little doubt that athletes can take practical steps, beyond becoming increasingly fit and acclimated to the heat, to prepare the gut for the rigors of competition. Adequate energy and fluid intake throughout each day, along with ingesting sufficient (not too little, not too much) fluid, carbohydrate, and electrolytes during exercise are perhaps the most critical steps athletes can take to optimize gut function during training and competition.
The majority of the GI-related complaints that beset athletes during exercise appear to be less due to limitations in gastrointestinal function than to mistakes that athletes make in fluid and energy intake. Avoiding volume depletion, hyperthermia, and excess energy intake helps preserve optimal gastric emptying, intestinal absorption, splanchnic blood flow, and membrane-barrier function.
Athletes who experience persistent gut-related problems such as diarrhea, abdominal pain, and bloody stool should be counseled to seek medical care. Because these symptoms may be related to ischemic bowel disease, athletes should also be educated to limit or cease physical activity until given physician's clearance to resume training.
References and Recommended Reading
Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance
1.•• Moses FM: Exercise-associated intestinal ischemia.Curr Sports Med Rep
An excellent overview, especially for the interested clinician, of the dangers of ischemic bowel disorders in athletes.
2. Eichner ER: Gut reactions: athletes' gastrointestinal problems.Sports Med Digest
3. Oktedalen O, Lunde OC, Opstad PK, et al.
: Changes in the gastrointestinal mucosa after long-distance running.Scand J Gastroenterol
4. Benyo R: Derek Clayton: the world's fastest marathoner.Runner's World
5. Shi X, Horn MK, Osterberg KO, et al.
: Gastrointestinal discomfort during intermittent high-intensity exercise: effect of carbohydrate-electrolyte beverage.Int J Sports Nutr Exerc Metab
6. Morton DP, Callister R: Characteristics and etiology of exercise-related transient abdominal pain.Med Sci Sports Exerc
7. Peters HP, Bos M, Seebregts L, et al.
: Gastrointestinal symptoms in long-distance runners, cyclists, and triathletes: prevalence, medication, and etiology.Am J Gastroenterol
8.•• Gisolfi CV: Is the GI system built for exercise?News Physiol Sci
A brief and very readable review of the physiology of GI function during exercise.
9. Murray R, Shi X: The gastrointestinal system.
In ACSM's Advanced Exercise Physiology. Edited by Tipton CM, Sawka MN, Tate CA, Terjung RL. Philadelphia: Lippincott Williams & Wilkins; 2005:357–369.
10. Rao SSC, Beaty J, Chamberlain M, et al.
: Effects of acute graded exercise on human colonic motility.Am J Physiol (Gastrointest Liver Physiol)
11. Rehrer NJ, van Kemenade MC, Meester TA, et al.
: Gastrointestinal complaints in relation to dietary intakes in triathletes.Int J Sports Nutr
12.• Van Nieuwenhoven MA, Brouns F, Brummer RJM: Gastrointestinal profile of symptomatic athletes at rest and during physical exercise.Eur J Appl Physiol
This study measured a variety of GI responses in athletes who were either symptomatic or asymptomatic for exercise-induced GI disturbances.
13. Sawka MN, Young AJ: Physiological systems and their responses to conditions of heat and cold.
In ACSM's Advanced Exercise Physiology. Edited by Tipton CM, Sawka MN, Tate CA, Terjung RL. Philadelphia: Lippincott Williams & Wilkins; 2005:535–563.
14. Boley SJ, Brandt LJ, Frank MS: Severe lower intestinal bleeding: diagnosis and treatment.Clin Gastroenterol
15. Takala J: Determinants of splanchnic blood flow.Br J Anaesth
16. Food Eating Contests and Records.
17.• Leiper JB, Nicholas CW, Ali A, et al.
: The effect of intermittent high-intensity running on gastric emptying of fluids in man.Med Sci Sports Exerc
For those interested in additional information on gastric emptying during exercise, this research paper offers an up to date overview.
18. Carrio I, Estorch M, Serra-Grima R, et al.
: Gastric emptying in marathon runners.Gut
19. Harris A, Lindeman AK, Martin BJ: Rapid orocecal transit in chronically active persons with high energy intake.J Appl Physiol
20.• Brouns F, Beckers E: Is the gut an athletic organ?Sports Med
A comprehensive review of gut function during exercise, with an emphasis on the physiologic reasons for GI discomfort.
21. Rehrer NJ, Janssen GM, Brouns F, Saris WH: Fluid intake and gastrointestinal problems in runners competing in a 25-km race and a marathon.Int J Sports Med
1989, 10(Suppl 1)
22. Brouns F, Saris WHM, Rehrer NJ: Abdominal complaints and gastrointestinal function during long-lasting exercise.Int J Sports Med
23. Jeukendrup A: Carbohydrate intake during exercise and performance.Nutrition
24. Smetanka RD, Lambert GP, Murray R, et al.
: Intestinal permeability in runners in the 1996 Chicago Marathon.Int J Sports Nutr