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Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Physiology of splanchnic blood flow during exercise
  5. Pathophysiology of changes in splanchnic blood flow during physical exercise
  6. Motility in the GI-tract during physical exercise
  7. Gastrointestinal absorption and gut permeability during physical exercise
  8. Clinical presentation and management of exercise-induced gastrointestinal symptoms
  9. Management of GI-symptoms during physical exercise
  10. Acknowledgement
  11. References

Background

The prevalence of exercise-induced gastrointestinal (GI) symptoms has been reported up to 70%. The pathophysiology largely remains unknown.

Aim

To review the physiological and pathophysiological changes of the GI-tract during physical exercise and the management of the most common gastrointestinal symptoms.

Methods

Search of the literature published in the English and Dutch languages using the Pubmed database to review the literature that focused on the relation between splanchnic blood flow (SBF), development of ischaemia, postischaemic endotoxinemia and motility.

Results

During physical exercise, the increased activity of the sympathetic nervous system (SNS) redistributes blood flow from the splanchnic organs to the working muscles. With prolonged duration and/or intensity, the SBF may be decreased by 80% or more. Most studies point in the direction of increased SNS-activity as central driving force for reduction in SBF. A severely reduced SBF may frequently cause GI ischaemia. GI-ischaemia combined with reduced vagal activity probably triggers changes in GI-motility and GI absorption derangements. GI-symptoms during physical exercise may be prevented by lowering the exercise intensity, preventing dehydration and avoiding the ingestion of hypertonic fluids.

Conclusions

Literature on the pathophysiology of exercise-induced GI-symptoms is scarce. Increased sympathetic nervous system activity and decreased splanchnic blood flow during physical exercise seems to be the key factor in the pathogenesis of exercise-induced GI-symptoms, and this should be the target for symptom reduction.


Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Physiology of splanchnic blood flow during exercise
  5. Pathophysiology of changes in splanchnic blood flow during physical exercise
  6. Motility in the GI-tract during physical exercise
  7. Gastrointestinal absorption and gut permeability during physical exercise
  8. Clinical presentation and management of exercise-induced gastrointestinal symptoms
  9. Management of GI-symptoms during physical exercise
  10. Acknowledgement
  11. References

Physical activity has both positive and negative effects on general health and the gastrointestinal (GI) tract. A positive effect on reduced incidence of colorectal carcinoma and complicated diverticulitis has been reported.[1, 2] On the down side, strenuous exercise may cause GI-symptoms in up to 70% and may even be the reason to stop with sport participation.[3, 4] The purpose of this article is to review the physiological and pathophysiological changes of the GI-tract during exercise, which are outlined in Table 1.

Table 1. Physiological and pathophysiological changes of the gastrointestinal tract during physical exercise
 Physiological changes during physical exercisePathophysiological changes during physical exercise
Splanchnic blood flow (SBF)

Decrease in SBF up to 80% of baseline

Aggravated by younger age, exercise intensity, and exercise duration, dehydration, high environmental temperatureCounteracted by ingestion of food/fluid

GI-ischaemia if > 50% decrease in SBF:

Mucosal damage; nutrient malabsorption, GI- bleeding, impaired gut-barrier function and increased GI-permeability

Dysmotility?

Reperfusion damage: mucosal damage, bacterial translocation

GI-motility, primary or secondary to GI-ischaemia

Decreased oesophageal peristaltic activity and lower oesophageal sphincter tone

Disruption of antroduodenal motility

Small bowel and colon: no consistent effect

Decreased oesophageal clearance & delayed gastric emptying leading to belching, reflux, nausea and vomiting.

Diarrhoea?

GI-secretion and absorption

GI-secretion probably unaffected.

Water absorption unimpaired.

Limited carbohydrate absorption

Osmotic diarrhoea during carbohydrate overload or hypertonic fluids.

We will specifically focus on the role of splanchnic blood flow reduction in the pathogenesis of exercise-induced GI-symptoms. Furthermore, we give advices for the management of the most common gastrointestinal symptoms.

Physiology of splanchnic blood flow during exercise

  1. Top of page
  2. Summary
  3. Introduction
  4. Physiology of splanchnic blood flow during exercise
  5. Pathophysiology of changes in splanchnic blood flow during physical exercise
  6. Motility in the GI-tract during physical exercise
  7. Gastrointestinal absorption and gut permeability during physical exercise
  8. Clinical presentation and management of exercise-induced gastrointestinal symptoms
  9. Management of GI-symptoms during physical exercise
  10. Acknowledgement
  11. References

In rest, the splanchnic organs receive 20% of the cardiac output, but only consume 10–20% of the available oxygen.[5] To a certain extent, blood may be safely redistributed from the splanchnic organs to the working muscles and skin.[6] The splanchnic vascular bed may therefore act as a blood giver to the circulation during exercise.

Sympathetic nervous system (SNS) activity is massively increased in response to exercise.[6] This causes increased splanchnic vascular resistance that may decrease splanchnic blood flow (SBF), despite the massive rise in cardiac output associated with physical exercise.[5, 7, 8] In fact, SBF can decrease by 80% during maximum intensity exercise.[5, 9]

The importance of the SNS activity was demonstrated in a study in healthy patients and patients with spinal cord injury at two levels (high or low). The effects of exercise with an arm-crank test at 50% of maximum oxygen uptake (further referred to as %VO2 max) on the portal vein flow and femoral artery, were measured. In normal patients and low level spinal cord lesions, a 30% reduction in portal vein flow was observed, but in high spinal cord injury (sympathetic denervation), the portal vein flow remained unchanged. The opposite effect was observed in the femoral artery blood flow; an increase in blood flow was only seen with sympathetic control.[10] A similar effect was seen in patients with sympathetic failure, diagnosed as pure autonomic failure and multiple system atrophy, where the superior mesenteric artery (SMA) blood flow was unchanged as well.[11]

The effect of exercise on the GI blood flow is dependent on various factors including exercise duration, environmental temperature, age, prandial state and trained status.

The effect of exercise duration on SBF was studied by Rehrer et al. in which volunteers exercised at 70% of VO2 max for 60 min. A gradual reduction in portal vein flow from 20% after 10 min to 80% after 1 h was observed (Figure 1).[9] A 30-min exercise test aimed at submaximal levels of approximately 70% of VO2 max was associated with 43% and 56% reduction of splanchnic blood flow measured with SMA flow and indocyanin green respectively.[12, 13]

image

Figure 1. Portal vein flow at rest and during 60 min of cycling exercise at 70% VO2 max in eight healthy volunteers. Data expressed as percentage resting value. * Significant compared with resting value. Figure used with permission from Rehrer et al.[9]

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The reduction in SBF during exercise is more pronounced in high temperatures.[14-16] Kenney et al. compared the effects of exercise at 60% VO2 max in 22 °C and 36 °C in young and older individuals. Exercising in 36 °C resulted in an additional 17% decrease in SBF compared with 22 °C at the same relative exercise intensity. This decrease in SBF was accompanied by an increase in plasma norepinephrin levels in both old and young patients, but young individuals had higher norepinephrin (NE) levels compared with older people during the same relative exercise intensity. This was associated with a more pronounced decrease in SBF at the same relative exercise intensity, suggesting that the splanchnic bed of young and elderly are still equally sensitive to NE.[14, 15]

The influence of trained status and exercise intensity on the decrease in SBF is complex. In trained patients, the exercise-induced decrease in SBF is lower compared with untrained individuals at the same absolute exercise intensity.[14] However, when focusing on relative exercise intensity (defined as the percentage of an individual's maximal oxygen uptake), no differences in response of SBF to exercise between trained and untrained individuals were found.[17]

The modulating effect of a meal on decrease of SBF with exercise was nicely demonstrated in a study by Qamar and Read.[13] In healthy volunteers, the changes in SMA blood flow were assessed using duplex ultrasound in fasting state and (i) after a 30 min exercise test, (ii) after a test meal (390 kcal) and (iii) the exercise test after ingestion of the test meal. The exercise test reduced the SMA flow by 43%, whereas SMA blood flow was increased by 60% after ingestion of the test meal. When this exercise test was combined with the meal, the SMA blood flow was actually increased by 40%. This strongly suggests the effects of exercise-induced splanchnic blood flow reduction can be counteracted by ingestion of food/fluid. These findings have been confirmed by Eriksen and Waaler.[18]

Limited data are available if other regulating factors are important in exercise-induced changes of SBF. Endothelin-1, a natural peptide, exhibits potent vasoconstrictor activity. The potential effect of Endothelin-1 as splanchnic vasoconstrictor was shown by Ahlborg et al. who demonstrated that infusion of Endothelin-1 during an exercise test exaggerated the exercise-induced decrease in SBF.[19] In a study in well-trained and untrained volunteers with 30 min exercise at 60% VO2 max, postexercise Endothelin-1 levels were elevated in the untrained healthy volunteers, but were decreased in trained athletes.[20] As many studies showed that the decrease in SBF is related to relative exercise level, irrespective of trained status, it is less likely that ET-1 plays a crucial role as regulator of postexercise SBF decrease.

It has been shown that vasopressin levels increase significantly during exercise, an effect that was further enhanced during dehydration. As infusion of vasopressin resulted in reduced splanchnic blood flow in septic and cardiac surgery patients, a causal relation seems plausible.[21-23] Still, whether the increased levels of vasopressin during exercise actually caused reduction of the splanchnic blood flow currently remains unknown.[24] The effect of angiotensin on SBF during exercise seems to be very limited.[25]

Although neuroendocrine hormones (like gastrin, motilin and Vasoactive Intestinal Peptide) have been shown to reduce SBF in animal models, the levels to accomplish these effects were higher than the levels observed in humans during exercise.[24, 25] It seems unlikely that these hormones play an important role in exercise-induced hypoperfusion of the GI-tract, although the number of reported studies and patients are very small.

In summary, from the available studies, the fact that the decrease in SBF during exercise is closely related to the exercise intensity and this is regulated by SNS activity can be appreciated . The exercise-induced decrease in SBF can been counteracted by ingestion of food/fluid.

Pathophysiology of changes in splanchnic blood flow during physical exercise

  1. Top of page
  2. Summary
  3. Introduction
  4. Physiology of splanchnic blood flow during exercise
  5. Pathophysiology of changes in splanchnic blood flow during physical exercise
  6. Motility in the GI-tract during physical exercise
  7. Gastrointestinal absorption and gut permeability during physical exercise
  8. Clinical presentation and management of exercise-induced gastrointestinal symptoms
  9. Management of GI-symptoms during physical exercise
  10. Acknowledgement
  11. References

The question is whether the exercise-induced decrease in SBF can result in (i) gastrointestinal ischaemia and (ii) functional disorders of the GI-tract. Furthermore, it remains unknown if this decrease can be held responsible for the development exercise-induced GI-complaints.

Splanchnic blood flow and GI-ischaemia

The relation between relative exercise intensity and SBF is remarkably similar among studies.[5, 7-9, 18, 19, 25, 26] After 30 min of exercise at 60–70% of VO2 max, reduction in SBF between 30% and 60% can be expected, whereas the longer duration at this level or higher the intensity levels, the decrease in SBF was up to 80% (Table 2). However, no human or exercise studies have been performed to correlate the decrease in SBF with the development of GI-ischaemia. In dogs and pigs, development of GI-ischaemia was observed when SBF fell below a critical minimum of about 40–50% of normal SBF.[27-29]

Table 2. Fasting splanchnic blood flow in response to exercise
ReferenceMethod/VesselSubjectsExercise intensity (%VO2 max), exercise modeDurationOutcomeaRemarks
  1. DU, duplex-ultrasound; IGD, indocyanine green dye elimination technique; CA, coeliac artery; SMA, superior mesenteric artery; PV, portal vein; %VO2 max, percentage of maximal oxygen uptake.

  2. a

    Compared with resting, fasting state.

  3. b

    Identical exercise protocol.

Exercise <10 min
Endo etal.[124]DU/SMA8 women40 Watt cycling4 minUnchanged 
Exercise 10–30 min
Rowell etal.[5]IGD/PV10 men26–97%, TreadmillUnknown−47 to −87%Heterogenous exercise intensity
Qamar and Read[13]DU/SMA8 men, 8 womenIntensity n.a., Treadmill uphill15 min−43%Measured immediately after exercise
Perko etal.[8]bDU/CA and SMA10 sex unknown75% Cycling15 min

CA: −50%

  SMA: −32%

1 measurement failure in CA
Perko etal.[8]bIGD/PV8 sex unknown75% Cycling15 min−43% 
Bergeron etal.[25]IGD/PV8 men70%, Cycling30 min−45% 
Bergeron etal.[25]IGD/PV8 men50%, Cycling40 min0% 
Peters etal.[26]DU/SMA12 men70%, Cycling60 min−50%Poor individual reproducibility
Rehrer etal.[9]DU/PV8 men70%, Cycling60 min−80%1 measurement failure, 3 measurements reaching ‘no flow’
Exercise > 60 min
Ahlborg etal.[19]IGD/PV6 men40%, Cycling120 min−52% 

The frequent occurrence of exercise-induced GI-ischaemia has been confirmed in several human studies. Nielsen et al. showed that rowing at maximal levels for 30 min caused severe gastric ischaemia in all six athletes.[30] We have shown that 30 min cycling in healthy volunteers, aimed at maximal level during the last 5–10 min, caused gastric ischaemia in 6 of 10 healthy volunteers.[31] Van Wijck et al. also observed that GI-ischaemia was present in all patients who cycled for 60 min at 70% V02 max.[32] In the latter study, Intestinal Fatty Acid Binding Protein (iFABP) was also measured as early serum marker for GI-ischaemia.[33] They observed a rise in iFABP preceded by development of GI-ischaemia as measured with gastric tonometry (Figure 2).[32]

image

Figure 2. Physical exercise (60 min at 70% VO2 max) results in splanchnic hypoperfusion and epithelial damage. (a) Gastric tonometry shows decreased splanchnic perfusion during and after exercise (GAPg-a > 0.8 kPa reflects GI-ischaemia) (b) Plasma I-FABP levels rise in response to exercise reflecting intestinal epithelial damage. (c) Significant correlation between I-FABP levels and splanchnic hypoperfusion (GAPg-a PCO2). Data are mean ± SEM. * P < 0.01, ** P < 0.001, *** P < 0.0001. Used with permission from van Wijck et al.[32]

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Strenuous exercise was associated with increased endotoxinemia.[34-36] Endotoxemia in humans, defined as lipo-polysaccharides (LPS) concentrations >5 pg/mL, has been reported not only following prolonged exercise (e.g. ultra-distance marathon) but also after a short bout of exhaustional exercise.[34, 36-38] Anti-LPS immunoglobulins are higher than normal in well-trained athletes, suggesting repeated leakage of small amounts of LPS during exercise.[34] These LPS data suggest increased intestinal permeability due to ischaemia, but to our knowledge have focused on this causal relationship.

Splanchnic blood flow and GI-motility

It has been shown in several shock models using rats, dogs and mice that change in SBF influences the motility of the GI-tract. Changes in motility patterns could potentially affect the mucosal blood flow via mechanic compression of the microcirculation, although the latter effect seemed to be mild.[39-44] Most models include either severe shock (>50% decrease in systemic blood pressure) and/or prolonged duration of ischaemia of up to 5 h, and their relevance to the pathophysiology of exercise-induced symptoms in humans remains highly unclear.[39-43, 45] Few human studies have focused on the relation between SBF/GI-ischaemia and motility disorders. Changes in motility may be present in both affected and non-affected surrounding bowel.[41, 43, 45] Eventually, motility normalised after reperfusion of an ischaemic bowel, although structural neuronal damage has been reported.[46] The available evidence from both animal and human studies supports the connection between decreased SBF and development of both dysmotility and GI-ischaemia, with postischaemic endotoxinemia. No studies are available that actually show a convincing relation between the development of GI-ischaemia and real-time development of GI-complaints. Otte et al. showed that a 10-min exercise test to maximal intensity in healthy volunteers resulted in gastrointestinal ischaemia, but did not result in the development of GI-symptoms.[31] We confirmed these observations in healthy, well-trained asymptomatic patients.[47] Thus, although decreased GI blood flow is present in most people exercising at submaximal levels for 30 min or more, or at maximal levels for shorter times, the relation with development of GI-complaints has not been established so far.

Motility in the GI-tract during physical exercise

  1. Top of page
  2. Summary
  3. Introduction
  4. Physiology of splanchnic blood flow during exercise
  5. Pathophysiology of changes in splanchnic blood flow during physical exercise
  6. Motility in the GI-tract during physical exercise
  7. Gastrointestinal absorption and gut permeability during physical exercise
  8. Clinical presentation and management of exercise-induced gastrointestinal symptoms
  9. Management of GI-symptoms during physical exercise
  10. Acknowledgement
  11. References

The effects of exercise on the oesophagus and stomach have been studied mainly in runners. Decrements in oesophageal peristaltic activity, decrease in lower oesophageal sphincter tone and increased transient lower oesophageal sphincter relaxation were observed. All factors may contribute to gastro-oesophageal reflux during exercise.[48-51] Exercise intensity, dehydration and hyperthermia may cause delayed gastric emptying by increased duodenal and decreased antral smooth muscle activity.[50, 52-55] Furthermore, it has been shown that gastric emptying rate may depend on the volume and energy content of the drink ingested during exercise as well.[56] Soffer et al. showed that exercise may disrupt the normal antroduodenal motility. They showed that an exercise intensity dependent interruption of the phase-3-like activity of the motor migrating complex in 2/16 patients exercising at 80% VO2 max and 5 of 8 at 90% VO2 max.[54] Finally, increased intra-abdominal pressure, e.g. during weightlifting, may expulse acidic fluids from the stomach into the oesophagus.[48]

The effects of exercise on the small bowel seem limited. Most studies demonstrated unchanged small bowel transit times with exercise, although one study found a moderate increase in small bowel transit time after mild exercise (15 min physical activity at 30% VO2 max) in healthy, recreationally active, men and women.[57] In contrast, small bowel transit remained unchanged after 3 h of exercise at 60% VO2 max in eight well-trained, asymptomatic cyclists[54] and in female long-distance runners with (n = 6) and without (n = 5) diarrhoea. No difference in small bowel transit time was found in rest and during 1 h exercise in neither symptomatic nor asymptomatic runners.[58] Unfortunately, the lactulosis breath test, used to measure the oral coecal transit time, might unpredictably influence the measurement outcome as both the hypertonic meal and lactulose may accelerate oral coecal transit time.[59] In the earlier mentioned study by Rao, no difference in colonic transit time between rest and exercise or symptomatic and asymptomatic subjects was found.[58]

Only one study reports on the immediate effects of colon motility during exercise. During short bouts of incremental exercise, a decrease in colonic motility was observed in 11 untrained patients using a solid state measurement probe. Colonic motility was quickly restored or increased immediate postexercise.[60] Two studies reported on colonic transit time with conflicting results. A reduced colonic transit time, and easier defecation, was found in sedentary, constipated patients after a 12-week period of daily 30 min brisk walking.[61] In a study in nonconstipated healthy but sedentary volunteers, a 9-week training schedule produced no changes in colonic transit time, and defecation was found, despite a marked increase in physical fitness.[62]

Gastrointestinal absorption and gut permeability during physical exercise

  1. Top of page
  2. Summary
  3. Introduction
  4. Physiology of splanchnic blood flow during exercise
  5. Pathophysiology of changes in splanchnic blood flow during physical exercise
  6. Motility in the GI-tract during physical exercise
  7. Gastrointestinal absorption and gut permeability during physical exercise
  8. Clinical presentation and management of exercise-induced gastrointestinal symptoms
  9. Management of GI-symptoms during physical exercise
  10. Acknowledgement
  11. References

The influence of exercise on gastrointestinal absorption depends on exercise intensity, nutritional status and the absorbed substances. Water absorption seems to be largely unaffected during normal physical exercise.[63, 64] The maximum absorptive capacity of the bowel for carbohydrate is estimated at 70–90 g/h and seems to be maintained during strenuous exercise.[65]

Several studies reported a reduced mucosal integrity of the bowel wall after exercise.[66, 67] Lambert et al. showed that the gastric and small bowel permeability damage was aggravated by the use of Non-Steroidal Anti-Inflammatory Drugs (NSAID).[68]

It was shown that water restriction during prolonged exercise worsened this intestinal permeability.[69] The results from the earlier mentioned study by van Wijck et al. strongly suggests that this increased intestinal permeability is related to mucosal damage secondary to GI-ischaemia.[32]

Clinical presentation and management of exercise-induced gastrointestinal symptoms

  1. Top of page
  2. Summary
  3. Introduction
  4. Physiology of splanchnic blood flow during exercise
  5. Pathophysiology of changes in splanchnic blood flow during physical exercise
  6. Motility in the GI-tract during physical exercise
  7. Gastrointestinal absorption and gut permeability during physical exercise
  8. Clinical presentation and management of exercise-induced gastrointestinal symptoms
  9. Management of GI-symptoms during physical exercise
  10. Acknowledgement
  11. References

Epidemiology of exercise-induced GI-symptoms

A summary of epidemiological studies reporting the incidence of exercise-induced GI-symptoms is presented in Table 3. The overall incidence in athletes varies from 45% to 81% depending on the definitions of ‘symptomatic’. The incidence and type of GI-symptoms depend on many factors such as type of sport, exercise intensity, (pre)competition food and fluid intake, age and gender.[4, 70, 71] The prevalence of GI-symptoms in the resting state may be an important factor as well.[4] GI-symptoms in rest may be the result of exercise-induced GI-symptoms, but may be pre-existent and (severely) increase during exercise.[72, 73] Upper GI-symptoms include regurgitation, chest pain, heartburn, belching, nausea and vomiting. Lower GI-symptoms include abdominal pain, flatulence, urge to defecate, diarrhoea and rectal bleeding.[4, 70, 74, 75] Lower GI-symptoms tend to occur more often in runners than upper GI-symptoms and in women.[4] In a large cohort of participants of the 2006 Enschede Marathon, the overall incidence of GI-symptoms was 19% in female runners compared with 8% in male runners.[71]

Table 3. The incidence of exercise-induced GI-symptoms
ReferenceType sportLevel of sportNumber of athletes addressed (response %)Overall incidence of GI-symptomsaIncidence of upper GI-symptomsbIncidence of lower GI-symptomsc
  1. n.a., not available.

  2. a

    All reported symptoms.

  3. b

    Nausea, heartburn, vomiting.

  4. c

    Cramps, urge to defecate, diarrhoea.

Keeffe et al.[125]RunningMarathon1700 (41)n.a23%66%
Worobetz and Gerrard[93]Multi-sportUltra-distance119 (59)81%58%61%
Riddoch and Trinick[126]Runningmarathon1750 (27)83%36%88%
Peters et al.[4]RunningMarathon177 (93)n.a.36%71%
 CyclingElite191 (84)n.a.67%64%
 TriathlonElite201 (71)n.a53%62
Peters et al.[127]Long-distance walking40–50 km/day480 (32)21%8%11%
Ter Steege et al.[71]RunningRecreative2076 (60)45%28%17%

Upper gastrointestinal symptoms

Upper GI-symptoms are reported in up to 40% in runners, but may rise to 70% in cyclists.[4] The incidence of reflux/heartburn is usually the highest of the upper GI-symptoms and is estimated between 15% and 20% in runners.[4] Furthermore, reflux symptoms may be affected by prandial state and type of sport.[48, 49] Soffer et al. studied reflux in eight trained cyclists exercising at 60, 70 and 90% VO2 max. Reflux episodes increased significantly at 90% VO2 max, but did not result in more severe GI-symptoms.[76]

The exercise-induced increase in intra-gastric pressure and disturbance in LES-function may cause GI-symptoms like heartburn, chest pain, belching and dyspepsia.[48, 50] The intragastric pressure may rise due to contraction of abdominal musculature and by ingestion of fluid and food, whereas carbohydrate containing beverage may induce transient lower oesophageal sphincter relaxation. Aerophagia that often accompanies tachypnea during exercise may aggravate upper GI-symptoms.[74, 77] Furthermore, hyperosmolar carbohydrate sport drinks delayed gastric emptying time in some well-designed studies in athletes.[78-81] Carrio et al. studied the gastric emptying time during exercise and basal state in marathon runners. Athletes emptied their stomach significantly faster than controls in both rest and during exercise suggesting an effect of training.[82] Indeed, athletes not accustomed to fluid/food ingestion, had a twofold risk in developing GI-symptoms compared with athletes who were accustomed to fluid/food ingestion during exercise.[71] As delayed gastric emptying during exercise may result in nausea, vomiting and side-stitch, the adaptation observed in athletes may protect against development of symptoms associated by delayed gastric emptying.

Side-stitch or exercise-induced transient abdominal pain

Side-ache, stitch and sub-costal pain (commonly referred to as exercise-induced transient abdominal pain or ETAP) are common during exercise.[73] Substantial research on ETAP has been performed by Morton and colleagues.

Exercise-induced transient abdominal pain was reported in 18% of the competitors in a recreational run, whereas 4% reported severe abdominal pain.[71] This observed incidence is comparable to a study in 848 runners in whom 27% experienced ETAP during a 14 km.[83] Morton et al. also showed that the incidence of ETAP is influenced by the type of sport. In 965 sporting participants, ETAP was most prevalent in activities that involved repetitive torso movements, bouncing or longitudinal rotation.[84] The incidence of ETAP was higher in young patients and after recent ingestion of fluid and food.[78, 85, 86]

The aetiology of ETAP remains to be fully elucidated. Proposed pathophysiological mechanisms include diaphragmatic ischaemia and stretch on visceral ligaments.[87-89] It has recently been shown that electromyographic activity of the abdominal muscle wall was not elevated during exercise in athletes suffering from ETAP compared with asymptomatic patients. This suggests that ETAP is not the result of muscle cramping either.[90] Morton et al. propose that ETAP is a form of peritonitis that may develop in two ways. First, extensive diaphragmatic excursion during exercise would result in decreased serous peritoneal fluid. Second, peritoneal fluid could be further reduced by ingestion of hypertonic fluid. This might result in irritation of the peritoneum due to friction of the visceral and parietal folds. Distension of the stomach and gut by food ingestion or torso movements could exacerbate the friction of the peritoneum.[91]

Lower GI-symptoms

Lower GI-symptoms include abdominal pain, flatulence, cramping and urge to defecate, diarrhoea and rectal bleeding. The exact incidence varies upon the type of sport and exercise intensity. Our research group found an incidence of 30% of severe lower GI-symptoms during a recreational run. However, this may increase up to 50% in cyclists and 70% in competitive long-distance runners.[73, 92, 93]

The pathogenesis of lower GI-symptoms is probably multifactorial. For example, diarrhoea during exercise may be provoked by incomplete bowel movement before starting exercise and mental stress. Furthermore, it has been suggested that increased GI-permeability, due to GI-ischaemia or NSAID, might also induce diarrhoea.[94, 69] Still, little evidence is available. The potential influence of GI-ischaemia was nicely illustrated by a case report by Desmond. An elite runner suffered from abdominal pain and diarrhoea after exercise. Compression of the coeliac artery by the median arcuate ligament was diagnosed. After surgical division of the constricting ligament, complete symptom relief was achieved.[95]

GI-bleeding and anaemia

Occult gastrointestinal blood loss and iron deficiency in athletes has a reported prevalence of 20%.[96-101] Microscopic and macroscopic gastrointestinal blood loss may be caused by e.g. haemorrhoids, colonic polyps and possibly by ischaemic mucosal damage.[92, 102, 103] Other potential pathogenic mechanisms of runner's iron deficiency and anaemia are expansion of plasma volume, traumatic haemolysis, haematuria and iron loss in sweat.[104-106] Acceleration/deceleration forces during running might result in hemorrhagic gastritis, haematuria and mechanic trauma to the colon, ‘coecal slap syndrome’, causing gastrointestinal blood loss.[70, 92, 103, 107]

The use of NSAID has been associated with a higher prevalence of occult blood loss and a higher amount of GI blood loss.[108] NSAID may result in additional ischaemic damage, either by blocking the synthesis of the vasodilating substance prostaglandin of by inducing mitochondrial damage.[109]

Massive and life threatening GI blood loss due to ischaemic colitis has been described in athletes.[110] Proximal, distal or pancolitis due to ischaemia, and even small bowel infarction after exercise have been reported, sometimes requiring major surgery.[111-113] It is conceivable that massive rectal bleeding and severe colonic ischaemia may only occur in extreme conditions like high exercise intensity in hot environment and severe dehydration in which massive splanchnic vasoconstriction is present. Probably, several warning signs (like cramping pain, diarrhoea and nausea) must be ignored before transmural ischaemia develops.[112]

GI-symptoms after physical exercise

Fever, shivering, nausea, vomiting and diarrhoea after physical exercise have been reported in up to 40% in endurance athletes.[4] In recreational runners, 11% reported GI-symptoms after a race, most often nausea (5%), shivering (5%) and diarrhoea (5%). It has been shown that athletes with symptoms during exercise have a fourfold risk on development of symptoms after physical exercise.[71] The literature available on GI-symptoms after physical exercise is very scarce. In animal studies, it has been shown that severe, reversible GI-ischaemia could result in long-lasting dysmotility, but this has not been studied in humans.[44] Furthermore, due to ischaemia/reperfusion damage, endotoxemia and increased serum lipopolysasccharide levels have been shown. In one study by Ashton et al., eight of ten volunteers had chills and nausea after exercise until exhaustion, and all had endotoxemia.[35] Heat stroke and collapse during exertion may be caused by endotoxemia as well.[114]

Management of GI-symptoms during physical exercise

  1. Top of page
  2. Summary
  3. Introduction
  4. Physiology of splanchnic blood flow during exercise
  5. Pathophysiology of changes in splanchnic blood flow during physical exercise
  6. Motility in the GI-tract during physical exercise
  7. Gastrointestinal absorption and gut permeability during physical exercise
  8. Clinical presentation and management of exercise-induced gastrointestinal symptoms
  9. Management of GI-symptoms during physical exercise
  10. Acknowledgement
  11. References

General principles

There is very little evidence for treatment or prevention of exercise-induced complaints. Most are based on experience or deduced from pathophysiological considerations, and are level V mostly. If an athlete presents with GI-symptoms during exercise, it should be ascertained that the symptoms are a sign of an underlying GI-disease. The widely given recommendations to reduce exercise-induced GI-symptoms include reduction of exercise intensity, prevention of dehydration and the use of isotonic fluids act at the level of SBF maintenance. Similarly, lowering the exercise intensity and prevention of dehydration may also help to maintain the splanchnic blood flow above the critical ischaemical level.[16] Avoidance of NSAID or COX- inhibitors use makes sense as discussed previously. It should be noted that up to 25% of the athletes uses these drugs on a regular basis.[115, 116]

It is important for athletes to train to ingest food and fluids before exercise, as it was shown to reduce the incidence of GI-symptoms besides its importance in maintaining the energy stores.[71, 82, 117] We showed that use of fluid and food in unaccustomed athletes resulted in a twofold risk on the development GI-symptoms.[71]

Reflux and regurgitation

The avoidance of heavy meals before exercise and hypertonic fluids during exercise reduces problems of gastric fullness and regurgitation.[78, 118]

Reflux can be treated by H2-blockers and proton pump inhibitors, with proven effect on frequency and duration of reflux time and pH in oesophagus during exercise.[119, 120] From a physiological point of view, a proton pump inhibitor may be of additional help for reduction of ischaemia, as it lowers the basal metabolism of the stomach, thereby reducing the oxygen demand.[121] However, this has not been proved in humans.

Lower GI-symptoms

The literature on the prevention of lower GI-symptoms is even rarer than for upper GI-symptoms. In literature, common sense’ advices are often provided such as to defecate prior to exercise to prevent the urge for defecation during exercise.[73] Furthermore, athletes should drink small amounts of hypotonic carbohydrate fluids to prevent the risk for osmotic diarrhoea.[65]

Side-stitch

For prevention of side-stitch or ETAP, several empirically based advices have been reported: (i) wait 2–3 h before exercising after a meal or drink, (ii) take small amounts of drink during exercise and refrain from hypertonic fluids in to reduce tugging of the gut on ligaments connecting the gut to the diaphragm. Only one clinical trial to prevent ETAP has been performed by Plunket et al. In a group of 10 athletes known with ETAP, tightening the abdominal muscles and breathing at a higher functional residual capacity alleviated side-stitch within seconds.[85]

Postexercise complaints

Very little evidence is available on how to prevent systemic and gastrointestinal symptoms after exercise. Ashton et al. showed in a small study that a high dose of the antioxidant ascorbic acid could abolish the exercise-induced increase in plasma LPS. Furthermore, the chills and nausea, experienced by the patients after exercise, could be prevented in eight of the ten studied patients by the ingestion of ascorbic acid.[35]

Persistent gastrointestinal complaints

In athletes with persistent symptoms despite these advices, duplex ultrasound of the coeliac artery and superior mesenteric artery might be performed to rule out obstructive splanchnic vessel disease. If present, a functional test like tonometry or visual light spectroscopy may be used to rule out the presence of GI-ischaemia in daily life, which may be a reason for treatment of the stenosis.[122, 123]

Although the presented studies strongly suggest a pivotal role for reduced splanchnic blood flow and ischaemia in the pathophysiology of exercise-induced GI-complaints, many links are still missing. The relation between changes in blood flow or development of ischaemia, and motility patterns are lacking. Similarly, more studies are needed to link the presence of GI-complaints on markers for ischaemia or motility disorders. These studies could guide therapeutic or prevention studies focused on reduction of exercise-induced GI-complaints.

In conclusion, from the limited available literature, it emerges that exercise leads to activation of the sympathetic nervous system, which triggers a reduction in splanchnic blood flow. With prolonged or maximal exercise levels, this reduced blood flow often results in GI-ischaemia. Although it seems likely that exercise-induced dysmotility and complaints are at least partially caused by ischaemia, no firm evidence is available. The literature on management of exercise-induced GI-symptoms is even more marginal, and advice is mainly based on authority-based evidence. Interestingly, many of these advices that were empirically based are aimed at maintaining the splanchnic blood flow, again suggesting a crucial role for GI-ischaemia in exercise-induced GI-complaints.

References

  1. Top of page
  2. Summary
  3. Introduction
  4. Physiology of splanchnic blood flow during exercise
  5. Pathophysiology of changes in splanchnic blood flow during physical exercise
  6. Motility in the GI-tract during physical exercise
  7. Gastrointestinal absorption and gut permeability during physical exercise
  8. Clinical presentation and management of exercise-induced gastrointestinal symptoms
  9. Management of GI-symptoms during physical exercise
  10. Acknowledgement
  11. References