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Sports Science Exchange (2013) Vol. 26, No. 114, 1-4

NUTRITIONAL RECOMMENDATIONS TO AVOID

GASTROINTESTINAL COMPLAINTS DURING EXERCISE
Erick Prado de Oliveira  | Center for Exercise, Metabolism and Nutrition   |   São Paulo State University |
Botucatu | Brazil
Asker Jeukendrup  |  Gatorade Sports Science Institute | Barrington (IL) | United States of America

KEY POINTS
• Gastrointestinal (GI) problems are very common, especially in endurance athletes, and often impair performance or subsequent recovery.
• Blood flow to the GI tract is impaired during exercise and this is believed to contribute to the development of GI symptoms.
• There are three main causes of GI symptoms: physiological (reduced blood flow to the gut), mechanical (bouncing effect of running, for example) or nutritional.
• The gut is sensitive to water and nutrient intake during exercise and to hypovolemia, hyperthermia, hypoglycemia, hypoxia and ischemia.
GAT11LOGO_GSSI_vert_fc_grn
• The information that is available suggests that gut permeability can be compromised in athletes; however, this has not yet been linked
conclusively to GI symptoms.
• GI symptoms among athletes vary enormously, and some athletes are more prone than others.
• Nutritional training and appropriate nutrition choices can reduce the risk of GI discomfort during exercise by assuring rapid gastric emptying and
absorption of water and nutrients, and by maintaining adequate perfusion of the splanchnic vasculature.
• Avoiding protein, fat, fiber and milk products can reduce the risk of developing GI symptoms during exercise.

INTRODUCTION Internet-based observational study in 1,281 athletes, 45% reported at

Gastrointestinal (GI) complaints are very common among endurance least one GI symptom (Ter Steege et al., 2008). Pfeiffer et al. (2011)
athletes. Anecdotally, GI problems are perhaps the most common reported severe GI distress ranging from 4% in marathon running and
cause of underperformance in endurance events. Depending on cycling up to 32% in Ironman races. It was demonstrated that there
the methodology used and the events studied, an estimated 30% to was a strong correlation between GI symptoms and having a history of
90% of distance runners experience intestinal problems related to GI symptoms (Pfeiffer et al., 2009; Pfeiffer et al., 2011), indicating that
exercise. These complaints may be of varying severity, but symptoms some people are more prone to develop GI symptoms and suggesting
may include nausea, vomiting, abdominal angina and bloody that there is a large genetic component to these problems. Clearly,
diarrhea. In many cases, these problems can have negative effects there is large variation in the reported prevalence in the literature
on performance and also have an impact on subsequent recovery. and this seems to be attributable at least in part to the method of
Bill Rodgers, a marathon legend, with four victories in both the investigation (the way GI symptoms are defined and recorded). In
Boston and New York City Marathons in the late 1970s, said, “More addition, however, the reported prevalence of these symptoms varies
marathons are won or lost in the portable toilets than at the dinner in different studies depending on the study population, sex, age and
table.” This illustrates the magnitude of the problem for endurance training status of the athletes, as well as mode and intensity of the
athletes and in particular long distance runners. This review will exercise studied, and the environmental conditions.
discuss the prevalence of GI complaints in athletes, discuss the
etiology of the problems and start to develop guidelines to prevent When analyzing the reported symptoms it becomes immediately
the issues. obvious that these symptoms are highly individual and there are no
clear patterns with regards to the type of activity and the types of
PREVALENCE OF GI PROBLEMS IN ATHLETES symptoms observed. There is a fairly large, yet well-defined number
One review stated that in exhausting endurance events, 30% to 50% of different GI symptoms that can occur during exercise. These
of participants may suffer from one or more GI symptom (Brouns & symptoms are summarized in Table 1. Generally the symptoms can
Beckers, 1993). A study in long distance triathletes who competed in be classified as either upper or lower GI tract symptoms. Typically
extreme conditions demonstrated a prevalence of up to 93% for any lower GI tract problems are more severe in nature, but all symptoms
one GI symptom (Jeukendrup et al., 2000). More alarming was that have the potential to impair performance.
43% of triathletes reported serious GI problems and 7% abandoned
the race because of GI problems (Jeukendrup et al., 2000). Among Symptoms are often mild and may not affect performance. Some of
elite endurance athletes the prevalence of exercise-induced GI the symptoms, however, can be very serious and will not only affect
symptoms was reported to be 70% (Peters et al., 1999) and in an performance, but can also threaten health.

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Table 1 nervous system induces splanchnic vasoconstriction. This will result

in an increase in the total splanchnic vascular resistance (Otte et
UPPER ABDOMINAL LOWER ABDOMINAL al., 2005; Wright et al., 2011), while at the same time the vascular
SYMPTOMS SYMPTOMS resistance in other tissues with increased activity during exercise
Reflux/heartburn Intestinal/lower abdominal (heart, lungs, active muscle, skin) is decreased (Otte et al., 2001;
cramps Qamar & Read, 1987). During maximal exercise, splanchnic blood
flow may be reduced by up to 80% to provide sufficient blood flow
Belching Side ache/stitch
to working muscle and skin. As blood is shunted from viscera to the
Bloating Flatulence active tissues (Qamar & Read, 1987), gut mucosal ischemia may
Stomach pain/cramps Urge to defecate (urgency) result as well as increase the mucosa permeability (Casey et al.,
Vomiting Diarrhea 2005). This in turn may be linked to nausea, vomiting, abdominal pain
Nausea Intestinal bleeding and diarrhea (De Oliveira & Burini, 2009; 2011), although convincing
evidence for this is lacking (Ter Steege & Kolkman, 2012).
SERIOUS SYMPTOMS
Among the reported deleterious manifestations of strenuous exercise CHANGES IN MOTILITY
are mucosal erosions and ischemic colitis, both observed after Changes in motility might be observed at different levels of the
long distance running (Heer et al., 1987; Choi et al., 2001; Moses, intestinal tract, including the esophagus, stomach and intestine.
2005). For example, marathon runners and long distance triathletes Decreases in esophageal peristaltic activity and lower esophageal
occasionally have blood loss in feces in the hours following a sphincter tone and increased transient lower sphincter relaxation
marathon. Schaub et al. (1985) observed epithelial surface changes have been observed and could be linked to gastroesophageal reflux
known to occur during ischemia upon colonoscopic inspection of one during exercise (Peters et al., 2000). Gastric emptying may also be
such triathlete following a marathon and suggested that ischemia of affected by exercise, although this probably only happens at high
the lower GI tract induced the problems (Schaub et al., 1985). Blood intensities of exercise or during intermittent activity (Leiper et al.,
loss as a result of ischemic colitis is not uncommon in athletes and 2001). Studies performed so far suggest that the effects of exercise
can be profound in extreme cases. Proximal, distal or pancolitis, and on the small bowel as well as the colon are limited.
even small bowel infarction have been reported in athletes and in
some cases required surgery (Heer et al., 1987; Lucas & Schroy, ABSORPTION AND GUT PERMEABILITY
1998). Despite the high prevalence of symptoms, mild or severe, Studies also suggest that there is little effect of exercise on intestinal
the etiology of these GI complaints in endurance athletes is still absorption of both water and carbohydrate (Lambert et al., 1997;
incompletely understood. Ryan et al., 1998). It must be noted, however, that the studies used
exercise intensities that were moderate and durations of exercise
CAUSES OF GI PROBLEMS that were no longer than two hours. It is feasible that during higher
While it is recognized that the etiology of exercise-induced GI exercise intensities, when blood flow to the intestine is compromised,
distress is multifactorial, GI ischemia is often acknowledged as and also after more prolonged exercise, that absorption is reduced.
the main pathophysiological mechanism for the emergence of the Oktedalen et al. (1992) reported increased intestinal permeability after
symptoms (Ter Steege et al., 2008; De Oliveira & Burini, 2011; Ter a marathon, indicating damage to the gut and impaired gut function.
Steege et al., 2011). The other factors are mechanical and nutritional There are numerous techniques available to study gut permeability
in nature. Below we will first discuss the physiological effects of but to date we have limited data. The information that is available
exercise that may contribute to the developments of GI symptoms. suggests that gut permeability can be compromised in athletes
(Pals et al., 1997). Although this has not been conclusively linked to
SPLANCHNIC HYPOPERFUSION gastrointestinal symptoms, one study showed that gut permeability
There is large heterogeneity in the response of the GI system to in symptomatic runners was greater than in asymptomatic runners
exercise. Splanchnic hypoperfusion (reduced blood flow) during (Van Nieuwenhoven et al., 2004). On the other hand, in one long
exercise ranges from mild circulatory changes to profound GI ischemia distance triathlon in extreme conditions where GI symptoms were
(Van Wijck et al., 2012). The consequences of hypoperfusion within highly prevalent, no compromised gut barrier function was observed
the GI tract, i.e., epithelial injury and changes in GI permeability as measured by bacterial translocation (LPS), a marker of mucosal
and epithelial barrier function, also differ greatly among individuals. damage and invasion of gram-negative intestinal bacteria and/
The presence and nature of abdominal symptoms experienced or their toxic constituents (endotoxins) into the blood circulation
by athletes vary from mild, exercise-related discomfort to severe (Jeukendrup et al., 2000). More research needs to be conducted
ischemic colitis and diarrhea (Moses, 1990). During strenuous before we have a clear understanding of the causes of GI distress.
physical activity or exercise, norepinephrine is released from nerve
endings and upon binding to α-adrenoreceptors of the sympathetic

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MECHANICAL CAUSES that was attributed to improved absorption. The training would have
The mechanical causes of GI problems are either impact-related reduced the chances of GI distress as improved intestinal absorption
or related to posture. For example, symptoms are more common in is generally associated with improved tolerance of fluids and foods
runners than in cyclists. This is thought to be a result of the repetitive during exercise (Jeukendrup & Mclaughlin, 2011).
high-impact mechanics of running and subsequent damage to
the intestinal lining. This repetitive gastric jostling is also thought OTHER CONTRIBUTING FACTORS
to contribute to lower GI symptoms such as flatulence, diarrhea It has been reported that large numbers of athletes use analgesics
and urgency. The mechanical trauma suffered by the gut from the to relieve existing or anticipated pain (Gorski et al., 2011). The use
repetitive impact of running, in combination with gut ischemia, likely of non-selective non-steroidal anti-inflammatory drugs (NSAIDs) has
account for GI bleeding. Posture can also have an effect on GI been associated with a three- to five-fold increased risk of upper
symptoms. For example on a bicycle, upper GI symptoms are more GI complications, mucosal bleeding or perforation compared to no
prevalent possibly due to increased pressure on the abdomen as a medication (Gabriel et al., 1991).
result of the cycling position, specifically when in the “aero” position.
“Swallowing” air as a result of increased respiration and drinking PREVENTION OF GASTROINTESTINAL PROBLEMS
from water bottles can result in mild to moderate stomach distress. In order to prevent GI distress, a few guidelines can be provided. It
In general, the only way to reduce the effects of these mechanical must be noted, however, that these are based on limited research.
causes is by training. Nevertheless, anecdotally these guidelines seem to be effective:
• Avoid milk products that contain lactose as even mild lactose
NUTRITIONAL CAUSES intolerance can cause problems during exercise. For instance it is
It is known that nutrition can have a strong influence on GI distress, possible to avoid milk completely or get lactose-free milk. Soy, rice
although many of the problems can persist in the absence of any and almond milks generally don’t contain lactose.
food intake prior to or during exercise. Fiber, fat, protein and fructose
• Avoid high-fiber foods in the day or even days before competition.
have all been associated with a greater risk to develop GI symptoms.
For the athlete in training, a diet with adequate fiber will help to keep
Dehydration, possibly as a result of inadequate fluid intake to offset
the bowel regular. Fiber before race day is different. By definition,
sweating, may also exacerbate the symptoms. A study by Rehrer et
fiber is not digestible, so any fiber that is eaten essentially passes
al. (1992), demonstrated a link between nutritional practices and GI
through the intestinal tract. Increased bowel movements during
complaints during a half-Ironman distance triathlon. Gastrointestinal
exercise are not desirable and will accelerate fluid loss. It may also
problems were more likely to occur with the ingestion of fiber, fat,
result in unnecessary gas production which might cause cramping.
protein and concentrated carbohydrate solutions during the triathlon.
A low-fiber diet the day before (or even a couple of days before) is
Beverages with high osmolalities (>500 mOsm/L) seemed to be
recommended, especially for those individuals who are prone to
associated with increased symptoms. The intake of dairy products
develop GI symptoms. Choose processed white foods, like regular
may also be linked to the occurrence of gastrointestinal distress
pasta, white rice and plain bagels instead of whole grain bread,
(De Vrese et al., 2001). Mild lactose intolerance is fairly common
high-fiber cereals and brown rice. Check the food labels for fiber
and could result in increased bowel activity and mild diarrhea.
content. Most fruits and vegetables are high in fiber but there are a
To minimize GI distress, all these risk factors must be taken into
few exceptions as zucchini, tomatoes, olives, grapes and grapefruit
account, and milk products, fiber, high fat and high protein must be
all have less than one gram of fiber per serving.
avoided 24 hours before competition and during exercise.
• Avoid aspirin and non-steroidal anti-inflammatory drugs
“TRAINING THE GUT” (NSAIDs) such as ibuprofen. Both aspirin and NSAIDs have been
It has been shown that athletes who are not accustomed to fluid shown to increase intestinal permeability and may increase the
and food ingestion during exercise had a two-fold risk of developing incidence of GI complaints. The use of NSAIDs in the pre-race period
GI symptoms compared with athletes who were accustomed to should be discouraged.
taking fluid and food during exercise (Ter Steege et al., 2008). The • Avoid high-fructose foods (in particular drinks that have exclusively
gut is highly adaptable and endurance athletes should incorporate fructose). Interestingly, however, fructose in combination with glucose
nutritional training into their training plans (Jeukendrup & Mclaughlin, may not cause problems and may even be better tolerated.
2011). This was nicely demonstrated in a study by Cox et al. (2010).
• Avoid dehydration since it can exacerbate GI symptoms. Start the
In this study, 16 endurance-trained cyclists or triathletes were pair-
race (or training) well hydrated.
matched and randomly allocated to either a high-carbohydrate group
(High group; n = 8) or an energy-matched low-carbohydrate group • Practice new nutrition strategies by experimenting with your pre-
(Low group; n = 8) for 28 days. It became apparent after 28 days race and race-day nutrition plan many times prior to race day. This
that the High group had higher exogenous carbohydrate oxidation will allow the athlete to determine what works and what does not work
rates during exercise than the Low group (Cox et al., 2010), a finding and also will reduce the chances of getting GI symptoms.

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CONCLUSION Moses, F. M. (2005). Exercise-associated intestinal ischemia. Curr Sports Med

Rep. 4:91-5.
The gut is an important athletic organ because it is responsible
for the delivery of water and nutrients during exercise. Both upper- Oktedalen, O., Lunde, O. C., Opstad, P. K., Aabakken, L. and Kvernebo, K. (1992).
Changes in the gastrointestinal mucosa after long-distance running. Scand J
and lower-gastrointestinal (GI) complaints are highly prevalent
Gastroenterol. 27:270-4.
among athletes during exercise (especially endurance athletes) and
Otte, J. A., Geelkerken, R. H., Oostveen, E., Mensink, P. B., Huisman, A. B.
can negatively impact performance. In severe cases it can pose and Kolkman, J. J. (2005). Clinical impact of gastric exercise tonometry
health risks too. Most GI complaints during exercise are mild and on diagnosis and management of chronic gastrointestinal ischemia. Clin
of no risk to health, but hemorrhagic gastritis, hematochezia and Gastroenterol Hepatol. 3:660-6.
ischemic bowel can present serious medical challenges. Nutritional Otte, J. A., Oostveen, E., Geelkerken, R. H., Groeneveld, A. B. and Kolkman, J. J.
training and appropriate nutritional choices can reduce the risk of (2001). Exercise induces gastric ischemia in healthy volunteers: a tonometry
GI discomfort during exercise by assuring rapid gastric emptying study. J Appl Physiol. 91:866-71.
and absorption of water and nutrients and by maintaining adequate Pals, K. L., Chang, R. T., Ryan, A. J. and Gisolfi, C. V. (1997). Effect of running
perfusion of the splanchnic vasculature. intensity on intestinal permeability. J Appl Physiol. 82:571-6.
Peters, H. P., Bos, M., Seebregts, L., Akkermans, L. M., Van Berge Henegouwen,
G. P., Bol, E., Mosterd, W. L. and De Vries, W. R. (1999). Gastrointestinal
REFERENCES
symptoms in long-distance runners, cyclists, and triathletes: prevalence,
Casey, E., Mistry, D. J. and Macknight, J. M. (2005). Training room management of
medication, and etiology. Am J Gastroenterol. 94:1570-81.
medical conditions: sports gastroenterology. Clin Sports Med. 24:525-40, viii.
Peters, H. P., Wiersma, J. W., Koerselman, J., Akkermans, L. M., Bol, E., Mosterd, W.
Choi, S. C., Choi, S. J., Kim, J. A., Kim, T. H., Nah, Y. H., Yazaki, E. and Evans, D.
L. and De Vries, W. R. (2000). The effect of a sports drink on gastroesophageal
F. (2001). The role of gastrointestinal endoscopy in long-distance runners with
reflux during a run-bike-run test. Int J Sports Med. 21:65-70.
gastrointestinal symptoms. Eur J Gastroenterol Hepatol. 13:1089-94.
Pfeiffer, B., Cotterill, A., Grathwohl, D., Stellingwerff, T. and Jeukendrup, A. E.
Cox, G. R., Clark, S. A., Cox, A. J., Halson, S. L., Hargreaves, M., Hawley, J. A.,
(2009). The effect of carbohydrate gels on gastrointestinal tolerance during a
Jeacocke, N., Snow, R. J., Yeo, W. K. and Burke, L. M. (2010). Daily training
16-km run. Int J Sport Nutr Exerc Metab. 19:485-503.
with high carbohydrate availability increases exogenous carbohydrate
oxidation during endurance cycling. J Appl Physiol. 109:126-34. Pfeiffer, B., Stellingwerff, T., Hodgson, A. B., Randell, R., Poettgen, K., Res, P. and
Jeukendrup, A. E. (2011). Nutritional intake and gastrointestinal problems
De Oliveira, E. P. and Burini, R. C. (2009). The impact of physical exercise on the
during competitive endurance events. Med Sci Sports Exerc. In review.
gastrointestinal tract. Curr Opin Clin Nutr Metab Care. 12:533-8.
Qamar, M. I. and Read, A. E. (1987). Effects of exercise on mesenteric blood flow
De Oliveira, E. P. and Burini, R. C. (2011). Food-dependent, exercise-induced
in man. Gut. 28:583-7.
gastrointestinal distress. J Int Soc Sports Nutr. 8:12.
Rehrer, N. J., Van Kemenade, M., Meester, W., Brouns, F. and Saris, W. H. M.
De Vrese, M., Stegelmann, A., Richter, B., Fenselau, S., Laue, C. and
(1992). Gastrointestinal complaints in relation to dietary intake in triathletes.
Schrezenmeir, J. (2001). Probiotics--compensation for lactase insufficiency.
Int J Sport Nutr. 2:48-59.
Am J Clin Nutr. 73:421S-429S.
Ryan, A. J., Lambert, G. P., Shi, X., Chang, R. T., Summers, R. W. and Gisolfi,
Gabriel, S. E., Jaakkimainen, L. and Bombardier, C. (1991). Risk for serious
C. V. (1998). Effect of hypohydration on gastric emptying and intestinal
gastrointestinal complications related to use of nonsteroidal anti-inflammatory
absorption during exercise. J Appl Physiol. 84:1581-8.
drugs. A meta-analysis. Ann Intern Med. 115:787-96.
Schaub, N., Spichtin, H. P. and Stalder, G. A. (1985). [Ischemic colitis as a cause of
Gorski, T., Cadore, E. L., Pinto, S. S., Da Silva, E. M., Correa, C. S., Beltrami, F.
intestinal bleeding after marathon running]. Schweiz Med Wochenschr. 115:454-7.
G. and Kruel, L. F. (2011). Use of NSAIDs in triathletes: prevalence, level of
awareness and reasons for use. Br J Sports Med. 45:85-90. Ter Steege, R. W., Geelkerken, R. H., Huisman, A. B. and Kolkman, J. J. (2011).
Abdominal symptoms during physical exercise and the role of gastrointestinal
Heer, M., Repond, F., Hany, A., Sulser, H., Kehl, O. and Jager, K. (1987). Acute
ischaemia: a study in 12 symptomatic athletes. Br J Sports Med.
ischaemic colitis in a female long distance runner. Gut. 28:896-9.
Ter Steege, R. W. and Kolkman, J. J. (2012). Review article: the pathophysiology
Jeukendrup, A. E. and Mclaughlin, J. (2011). Carbohydrate ingestion during
and management of gastrointestinal symptoms during physical exercise, and
exercise: effects on performance, training adaptations and trainability of the
the role of splanchnic blood flow. Aliment Pharmacol Ther. 35:516-28.
gut. Nestle Nutr Inst Workshop Ser. 69:1-12; discussion 13-7.
Ter Steege, R. W., Van Der Palen, J. and Kolkman, J. J. (2008). Prevalence of
Jeukendrup, A. E., Vet-Joop, K., Sturk, A., Stegen, J. H., Senden, J., Saris, W. H. and
gastrointestinal complaints in runners competing in a long-distance run: an internet-
Wagenmakers, A. J. (2000). Relationship between gastro-intestinal complaints
based observational study in 1281 subjects. Scand J Gastroenterol. 43:1477-82.
and endotoxaemia, cytokine release and the acute-phase reaction during and
after a long- distance triathlon in highly trained men. Clin Sci (Colch). 98:47-55. Van Nieuwenhoven, M. A., Brouns, F. and Brummer, R. J. (2004). Gastrointestinal
profile of symptomatic athletes at rest and during physical exercise. Eur J
Lambert, G. P., Chang, R. T., Xia, T., Summers, R. W. and Gisolfi, C. V. (1997). Absorption
Appl Physiol. 91:429-34.
from different intestinal segments during exercise. J Appl Physiol. 83:204-12.
Van Wijck, K., Lenaerts, K., Grootjans, J., Wijnands, K. A., Poeze, M., Van Loon, L.
Leiper, J. B., Prentice, A. S., Wrightson, C. and Maughan, R. J. (2001). Gastric
J., Dejong, C. H. and Buurman, W. A. (2012). Physiology and pathophysiology
emptying of a carbohydrate-electrolyte drink during a soccer match. Med Sci
of splanchnic hypoperfusion and intestinal injury during exercise: strategies for
Sports Exerc. 33:1932-8.
evaluation and prevention. Am J Physiol Gastrointest Liver Physiol. 303:G155-68.
Lucas, W. and Schroy, P. C., 3rd (1998). Reversible ischemic colitis in a high
Wright, H., Collins, M., Villiers, R. D. and Schwellnus, M. P. (2011). Are splanchnic
endurance athlete. Am J Gastroenterol. 93:2231-4.
hemodynamics related to the development of gastrointestinal symptoms in
Moses, F. M. (1990). The effect of exercise on the gastrointestinal tract. Sports ironman triathletes? A prospective cohort study. Clin J Sport Med. 21:337-43.
Med. 9:159-72.