Aetiology of Running-Related Gastrointestinal Dysfunction

Aetiology of Running-RelatedGastrointestinal DysfunctionHow Far is the Finishing Line?

Susana M. Gil, Etsuro Yazaki and David F. EvansSt Bartholomew’s and the Royal London School of Medicine and Dentistry, London, England

Abstract 30 to 65% of long distance runners experience gastrointestinal (GI) symptomsrelated to exercise. Several hypotheses have been postulated; however, the aeti-ology and pathophysiology are far from clear.

The mechanical effect of running on the viscera must be involved in the devel-opment of GI symptoms in this sport. Reduction of splanchnic blood flow due tovisceral vasoconstriction is another widely supported theory; nevertheless, it doesnot explain many of the clinical findings. Examination of the GI tract duringexercise is a difficult task, and measurements of both orocaecal and whole-guttransit time have shown equivocal results. GI hormones, and especially prosta-glandins, may be of crucial importance for the production of symptoms. Intestinalabsorption, secretion and permeability may also be altered during exercise, pro-voking intestinal dysfunction. Factors such as stress, diet, dehydration, infectionsand other factors need to be analysed in order to present a global view of the hypo-theses regarding the aetiology of this common and often overlooked problem.

LEADING ARTICLE Sports Med 1998 Dec; 26 (6): 365-3780112-1642/98/0012-0365/$07.00/0

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1. Incidence of Gastrointestinal (GI)Disturbances Related to Exercise

Since the introduction to the literature of theterm ‘runner’s diarrhoea’ in the 1970s and 1980s,[1,2]

many attempts have been made to specify the inci-dence of gastrointestinal (GI) disturbances relatedto running. Although their results (based on sur-veys and questionnaires voluntarily answered byathletes) may be biased, most studies show that GIsymptoms are a common feature among long dis-tance runners.

Lower GI symptoms (diarrhoea, urgency, theneed to stop for a bowel movement, rectal inconti-nence, rectal bleeding and abdominal cramps) aremore commonly experienced than upper GI symp-toms (heartburn, reflux, nausea).[3-5] The latter are

more likely to occur at rest and in sedentary indi-viduals.[6]

The most common complaint is the urge to def-ecate while running, affecting 36 to 63% of run-ners,[3-5,7,8] whereas diarrhoea is experienced by 8to 54%[4,5,7-9] and abdominal cramps are experi-enced by about a third of the athletes involved inthis sport.[3-5,7-10] The need to stop to move thebowels occurs in 16 to 62% of runners and rectalbleeding and incontinence in 2 to 16%.[4,5,7-9]

Women were more severely affected in 2 sur-veys[4,5,7,8] and less than half believed that GIsymptoms were aggravated during the time of theirmenses.[6] Young athletes had more GI distur-bances than older runners in 2 studies.[5,7]

The relationship with the intensity of running isinconclusive: 2 reports found a positive relation-ship between the intensity of exercise and the

symptoms,[5,10] while another 3 studies failed todemonstrate any connection.[6,7,9]

The incidence of irritable bowel syndrome andalso lactose intolerance is similar to that in studiesof other populations (13 to 16%).[6,8,9] Pre-race di-arrhoea occurs in 40% of athletes; it is more com-mon in women and in those with irritable bowelsyndrome or lactose intolerance.[9]

Running appears to cause a greater degree of GIdisturbance than other activities involving high en-ergy output. During triathlon events, GI complaintsare generally more frequent than musculoskeletalinjuries, and stitch, bowel dysfunction, abdominalcramps and gastroesophageal reflux have been re-ported to be more common during the runningstages than in the swimming and cycling events.[10]

2. Aetiology of GI Dysfunction

2.1 Mechanical Factors

GI symptoms prevail in running compared withother sports where the body remains in a more sta-ble position, such as cross-country skiing, swim-ming or cycling.[11] The pounding effect or intesti-nal jarring is widely cited as a positive direct causefor the development of exercise-related GI symp-toms.[11-14] Rehrer and Meijer[15] measured the me-chanical vibration of the body using an exerciseaccelerometer and found that acceleration/deceler-ation was more than doubled in running comparedwith cycling.

This mechanical theory is supported by the ob-servation that GI disturbances are experiencedmainly during the running part of triathlon events[10]

and the running stages of a study of alternate run-ning and cycling.[16]

On the other hand, mechanical stimulation ofthe intestinal mucosa by rubbing[17] and disten-sion[18,19] releases vasoactive intestinal peptide (VIP)and prostaglandins (PG) [see sections 2.3 and 2.4],causing intestinal secretion which may produce asecretory type of diarrhoea.

Following the report of a runner with right ab-dominal pain on palpation and diarrhoea after amarathon race, the ‘caecal slap syndrome’ was intro-

duced.[20] The same author later admitted that therunner had ingested nonsteroidal anti-inflammatorydrugs (NSAIDs) and a small amount of alcohol.The interaction of these factors was questioned,[21]

but the caecal slap became a widely used hypothe-sis.

Hypertrophy of the psoas muscle, pressing onthe GI tract, has also been postulated as a cause ofGI symptoms due to running.[22]

Two competitive runners who presented withGI symptoms after exercise were intraoperativelyfound to have a caecal volvulus and also a thinmesentery. The ‘up and down’ movement of ab-dominal viscera while running was thought to bethe cause of the volvulus and the symptoms.[23]

GI complaints have not been reported in othersports such as boxing, horse riding, dancing ortrampolining, where theoretically a bouncingmovement of the intestinal contents would occur:however, this may not be entirely due to the factthat they do not occur, but rather that such distur-bances have not been investigated in these activi-ties. A prospective, structured questionnaire-basedstudy of GI disturbances in a wide variety of sport-ing activities is lacking but would help to increaseour understanding of the prevalence of this condi-tion.

2.2 Mesenteric Circulation and Exercise

2.2.1 Exercise-Associated GI BleedingGI bleeding is not an uncommon finding after

long distance races. Macroscopic faecal blood isexperienced by 1 to 16% of runners[6-9] and micro-scopic bleeding has been found in 8 to 87% of run-ners.[24-29] This wide range in the latter inci-dence may be due to differences in the length ofthe events after which faecal blood was measured.Using qualitative techniques after 42.6km mara-thon races[25,27,28,30-32] and a short triathlon,[33] 8 to36% of runners converted from negative to positivefaecal blood, whereas in much longer events suchas a 100-mile (160.9km) ultramarathon[26,28] anda long triathlon of 3.8km swim, 180km ride and42.2km run,[24] 80 to 87.5% of athletes had micro-scopic bleeding.

366 Gil et al.

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Using quantitative tests, the amount of faecalhaemoglobin increases in 71 to 83% of athletesafter marathon running,[27,34] whereas using animmunochemical technique (‘OC-Hemodia’) 33%of marathon finishers had positive faecal occultblood on the first post-race stool specimen.[35]

By comparison, lower results were observed incyclists during a 1 week cycling race, of whom 1.2%had positive findings.[36] In a different study, a37km walk on 4 consecutive days did not produceany changes in the amount of faecal haemoglo-bin.[27]

Faecal blood loss occurs more frequently aftera race than during training,[37,38] but no relation-ship has been found between faecal blood loss andfinishing times,[24,27-29,36] age,[25,27,29,30] sex,[29,30]

weekly mileage[25-28] or training experience.[28] Theappearance of blood in stools is correlated withlower GI disturbances.[25,28,35] Nonetheless, thisfinding is not consistent in all reports.[29,30,39]

Not only is the ingestion of aspirin (acetylsali-cylic acid) and NSAIDs unrelated to the incidenceof occult GI bleeding in runners,[26,29] but in somecases it offers a degree of protection. Runners tak-ing such medicines have fewer positive results thannonmedicated athletes after races.[28,32,36] Thus,PG may have an important role in the productionof GI bleeding related to exercise.

The effect of histamine H2 receptor antagonistson running-associated faecal bleeding is inconclu-sive. During a prospective study in a marathonrace, cimetidine reduced slightly, but not signifi-cantly, the incidence of positive faecal occult blood(FOB) using ‘Hemoccult’ tests. The incidence re-mained similar to that in other reports wheremedication was not taken.[25,27,28,30-32] With ‘Hemo-Quant’ tests, the amount of FOB in cimetidine re-cipients did not differ from that found in the run-ners taking a placebo.[39]

During an ultramarathon, 87.5% of runners nottaking cimetidine had positive FOB, whereas ofthose who were voluntarily taking the drug, 11%had blood in the stools.[26] The only difference inthese 2 groups of runners was that the first hadmore running experience; perhaps to avoid dehy-

dration they drank more water during the race, pro-ducing more hydrated faeces and giving more falsepositive results.[40]

However, all these results need careful interpre-tation. Qualitative tests (‘Hemoccult 11’, ‘Hema-Chek’, ‘Hemofec’ measure haemoglobin peroxi-dase activity and can produce false positive resultsin the presence of animal blood, vegetables, stoolhydration, ferrous sulfate and cimetidine,[27,35,40,41]

and false negative results with ascorbic acid, ant-acids and gut enzymes and bacteria.[27,40,42] Quan-titative tests, such as ‘HemoQuant’, are based onthe conversion of nonfluorescing haem to fluoresc-ing porphyrins[43] and may be affected by alter-ations of gut transit time.[37]

Running-related GI changes have been obser-ved endoscopically[29,44-47] and intraoperatively[48-49]

as gastric antral ulcer,[50] haemorrhagic gastritis,[44]

erosive gastritis,[29] ischaemic colitis,[47,49] non-specific colitis[48] and haemorrhagic colitis.[51] Histo-logical findings include decreased gastric mucosalsecretions, oedema, congestion, capillary dilationand red cell extravasation.[29,46-47] Such findingsare transient[13,32,35] and occur in the immediatepostexercise period,[46] improving with reductionof the amount of training,[47] rest[44,51,48] and theadministration of cimetidine/ranitidine.[45,50] Insome cases a full diagnostic GI series failed toshow any abnormalities in the GI tract.[29,52,53] Thiscould have been due to the time lapse between theGI bleeding and the diagnostic investigations,which were performed 4 to 11 days after the bleed-ing episode.

2.2.2 Reduction of Splanchnic Blood FlowExercise produces vasoconstriction of the

splanchnic vascular bed by the action of noradren-aline (norepinephrine) on the α-adrenoceptors viathe sympathetic nervous system.[54] This stimula-tion increases blood flow to the working musclesand skin (for thermoregulation) and maintainsblood flow to the heart and brain.[55,56] Table Ishows the effect of different types and intensitiesof exercise on mesenteric blood flow. As can beseen from table I, using the indocyanine green(ICG) hepatic clearance technique, estimated

Running-Related GI Dysfunction 367


splanchnic blood flow (SBF) decreases in aninversely proportional manner in relation to thepercentage of maximal oxygen consumption(V

.O2max) achieved,[57-60,62-63] duration of exer-

cise[60,62,63] and ambient heat.[58-60] Estimated he-patic blood flow (EHBF) with low intensity exer-cise (30 to 35% V

.O2max) is decreased by 12 to

14%[60] or unchanged;[64] with more severe exer-cise (35 to 60% V

.O2max) it decreases by 30 to 45%

for exercise lasting less than 50 minutes, and moreif the exercise lasts longer.[60,62,63]

Rowell et al.,[57] in their widely cited paper, es-timated that EHBF decreases by approximately80% of resting values during exercise; nonetheless,this was calculated by extrapolating the resultsfrom the ICG clearance due to the difficulties inobtaining hepatic venous samples during high in-tensity exercise. Such results have not been repro-

duced using the same technique, even when volun-teers approached exhaustion with attendant nauseaand vomiting.[59] Using other techniques, differentresults have been produced. Portal vein blood flowwas measured in moderately trained cyclists usingDoppler ultrasound techniques. After 20 minutesof cycling at 70% V

.O2max, SBF decreased by 57%,

and after 1 hour, by 80%. In 2 volunteers the SBFactually approached zero, therefore, the methodol-ogy must be questioned.[65]

Severe exercise (15 minutes at 5 km/h, 20% in-cline) reduced blood flow of the superior mesen-teric artery (SMA) by 43% from resting values.[66]

Abdominal blood flow measured by 99technetium-labelled red cells decreased to 96, 88 and 81% ofresting values at 50, 70 and 100% of maximumoxygen uptake.[67]

Table I. Effect of different types and intensities of exercise on the mesenteric blood flow

Population Exercise type Method Results Reference17M untrained 3.5 mph × 4.5 min, 7 mph to exhaustion ICG CL EHBF ↓ at ↑ V

.O2max 57

11M untrained 3.5 mph × 4.5 min at 25 and 43°C ICG CL EHBF ↓ at ↑ V.O2max and at 40°C 58

11M7 sedentary, 4 active

3.5 mph × 4.5 min at 48-48.9°C and 50% V

.O2max

ICG CL Small ↓ EHBF↑ O2 consumption

59

12M6 young (20-32y,sedentary)6 elderly (59-71y, fit)

20 min at 35% V.O2max, 30 min at

60% V.O2max, at 22 and 36°C

ICG CL 35%: SBF ↓ 12-14% (22 and 36°C; young and elderly)60% at 36°C young: SBF ↓ 45%, elderly: SBF ↓ 33%60% at 22°C young: SBF ↓ 31%, elderly: SBF ↓ 36%

60

13M Arm or leg training for 15 min/day over 5wk (mean heart rate of 130 and 170 bpm, respectively)

ICG CL ↓↓ EHBF with nontrained muscles arm > leg

61

6M 130 min cycling at 50% V.O2max,

140-150 bpmICG CL SBF ↓ 43% (more after 50 min) 62

20M 58% V.O2max × 3.5h ICG CL SBF ↓ 45% at 40 min; ↓ 20% at 90 min

O2 ↑ 70% at 40 min63

6sedentary

4h at 30% V.O2max, 129 bpm ICG CL EHBF ↔

O2 uptake ↑ 120% at 180 min64

8moderately trainedcyclists

Cycling at 70% V.O2max Portal vein USS

Doppler20 min ↓ 57%1h ↓ 80%2 individuals = 0

65

16M 15 min × 5 km/h walk SMA USSDoppler

↓ 43% SMA postexercise 66

14 (4F, 10M)4 sedentary, 10 active

Cycling: 50% × 10 min, 75% × 15 min,100% × 20 min

99Technetium-labelled red cells

Abdominal blood flow ↓ 96%, 88% and 81% of baseline, respectively

67

bpm = beats/min; EHBF = estimated hepatic blood flow; F = female; ICG CL = indocyanine green clearance; M = male; mph = miles/hour;SBF = splanchnic blood flow; SMA = superior mesenteric artery; USS Doppler = Doppler ultrasonography; V

.O2max = maximal oxygen

consumption; ↓ = decreased; ↓↓ = greatly decreased; ↑ = increased; ↑↑ = greatly increased; ↔ = unchanged; > = more than.

368 Gil et al.


Training attenuates the reduction of SBF,[61]

possibly due to adaptation of the sympathetic nerv-ous system.[68] Young, untrained men have agreater reduction than older fit men,[60] but it is notknown whether the different response is due to theage or the fitness of the participants.

Increased blood flow raises the rate of absorp-tion of substances by reducing their concentrationin the interstitial space.[69] Therefore, a decreasedblood flow may reduce absorption and the washouteffect of the substances of the interstitial fluid;hence, more substances accumulate in the colon,producing an osmotic effect with possible diar-rhoea and GI dysfunction.

Hypoperfusion and ischaemia of the splanchnicregion produced during cardiopulmonary bypassoperations reduce the permeability of 3-O-methyl-D-glucose (3-MG), mediated by an active andpassive carrier and D-xylose, and increase thepermeability of lactulose [absorbed through tightjunctions, adenosine triphosphate (ATP)-depend-ent]. Thus, decreased blood flow to the mesentericarea may impair the permeability and absorptionof some carbohydrates, thereby increasing levelsof these substances in the lumen and producingdiarrhoea.[70]

This theory is also supported by the fact that80% of marathon finishers with more than 4% ofweight loss due to dehydration experienced GI dis-turbances.[71] Dehydration reduces blood volume,possibly aggravating the reduction of splanchnicblood flow.

Experimental ischaemia of the GI tract, due toan impaired delivery of oxygen and metabolites,reduces cellular cytochromes,[72,73] mitochondrialrespiratory chains[72] and nucleotides,[73] produc-ing morphological and functional derangement ofthe mucosa and ultimately necrosis in mucosalgastric cells,[72] hepatocytes[73] and intestinalcells.[72,74-77] During reperfusion after ischaemia,more damage occurs due to the release of oxygen-derived free radicals.[78-80] Another possible mech-anism involved is the renin-angiotensin axis, whichconstricts mesenteric vessels during experimental

hypovolaemia[81-84] and is increased during exer-cise[85,86] in an intensity-dependent fashion.[87]

Moreover levels of endothelin, which is a potentsplanchnic vasoconstrictor[88,89] and produces mu-cosal damage and ischaemia,[90,91] are increasedduring dehydration[92] and exercise.[93] This is in-dependent of the duration and the intensity of theexercise.[94]

These mechanisms are also thought to be respon-sible for the stress ulceration found in patients withsevere trauma, major operations or thermal burns.[72]

The physiological splanchnic vasoconstriction as-sociated with exercise has been compared with theresponse occurring in these patients,[11,14,16,95] butthere are a number of differences:(1) Such severely ill patients have profound hypo-tension and decreased stroke volume whereas dur-ing exercise, blood pressure (particularly systolic),stroke volume and cardiac output are increased.[96]

Significant ischaemia is unlikely to occur inhealthy, trained, well hydrated runners.[97] On theother hand, nonocclusive ischaemic colitis is asso-ciated with haemorrhagic shock, low cardiac out-put, aortic stenosis, aortic insufficiency, acutemyocardial infarction, myocardiopathies, conges-tive cardiac failure and hypovolaemia.[98] None ofthese predisposing factors is present in the athleteswith running-associated colitis.[48,49,51]

(2) Physical endurance training is associated withan adaptive reduced sympathetic activity, which isindicated by lower basal and exercise catechola-mine levels in plasma.[56,68,99]

(3) Continuing stimulation of regional sympatheticnerves produces first a constrictor effect, followedby an ‘autoregulatory response’ (with partial or to-tal recovery of blood flow) and a hyperaemic phaseafter the cessation of the stimulation.[54]

In addition, reduction of the mesenteric bloodflow may be an important factor in the productionof GI disturbances associated with exercise, but onits own it fails to explain other clinical findings.

Postprandially, mesenteric blood flow is in-creased,[54] and the ingestion of food attenuates thereduction of blood flow induced by moderate tosevere exercise.[66] It would be expected that the



administration of food during exercise wouldimprove symptoms; however, runners as a rule vol-untarily abstain from exercise in the 3- to 5-hourpostprandial period.[5,7,10]

In addition, GI disturbances, should the reduc-tion of SBF be the main factor responsible, wouldoccur more commonly in higher intensity sportsand events, where the athletes reach higher heartrates and V

.O2max, such as middle distance races.

However, exercise-related diarrhoea, urgency andparticularly GI bleeding occur more frequently inmarathon and ultramarathon races where oxygenuptake and heart rate are far from reaching theirmaximum values.

Furthermore, some runners experience abdomi-nal distress at the beginning of a run[9] when bloodflow to the viscera should, theoretically, not becompromised.

2.3 Hormones

Gastrin, motilin, somatostatin, glucagon, pan-creatic polypeptide and VIP, which are increasedduring exercise,[100] may produce GI symptoms viadifferent mechanisms.

2.3.1 Vasoactive Intestinal Polypeptide (VIP)Mesenteric ischaemia[101] and mechanical stim-

ulus of the intestinal mucosa[19,102] evoke VIPrelease. VIP is a powerful stimulant of intestinalsecretion,[103,104] promotes colonic contraction, de-creases intestinal absorption in the dog[103] andprovokes a secretory type of diarrhoea.[105-107]

2.3.2 MotilinMotilin initiates migrating motor complexes[108]

and stimulates contraction of the intestinal musclefrom the rabbit[109] and human in vivo[110] and invitro.[111]

2.3.3 Peptide YYDuring exercise, splanchnic vasoconstriction is

associated with local release of peptide YY[112]

which increases small intestinal motility and con-traction.[113]

2.4 Prostaglandins (PG)

Eicosanoids are metabolites originating fromthe conversion of membrane phospholipids toarachidonic acid and the subsequent metabolisminto cyclooxygenase products (PG, thromboxanesand prostacyclin) and lipoxygenase products(leukotrienes). Mechanical stimuli[114] and smoothmuscle stretch[115,116] release PG. Thus, runningand the ‘up and down’ movement of the abdominalviscera stretching and distending the intestinal wallmay be responsible for the increase in systemic PGfound after marathon races.[117]

Evidence of increased PG synthesis can be dem-onstrated for virtually every recognised diarrhoeaillness.[118] PGE and PGF accelerate intestinal tran-sit time[119] and inhibit colonic contraction.[120,121]

In the dog, PGE2 induces giant migrating contrac-tions often associated with defecation.[122]

On the other hand, PGE2 decreases lower oe-sophageal sphincter pressure and oesophageal con-tractions.[123] PG stimulates intestinal fluid andelectrolyte accumulation in the gut lumen (en-teropooling effect) producing secretory diarrhoea,vomiting[124] and cramps.[118]

Runners taking NSAIDs and aspirin (both in-hibitors of PG production) have less positive FOBafter running than their nonmedicated counter-parts.[28,32,36]

In addition, loperamide, which is frequentlyused by runners to alleviate their symptoms, abol-ishes PG-induced diarrhoea.[125] Calmodulin, a cal-cium binding protein, mediates metabolism frommembrane phospholipids to arachidonic acid andsubsequently PG and leukotrienes. One of the anti-diarrhoeal effects of loperamide is obtained byblocking calmodulin.[126]

Therefore, running-associated vomiting, ab-dominal cramps, diarrhoea, urge to defecate andgastroesophageal reflux may be explained by anincreased production of PG by the GI tract. Fur-thermore, GI histological changes and GI bleedingmay be due to the release of leukotrienes (LCT4),which produce intense vasoconstriction of venulesand arterioles, leading to sluggish blood flow, cap-illary stasis, plasma leakage[127,128] and damage to

370 Gil et al.


measurements have not yet been made on athleteswith GI symptoms.

2.6.2 Colonic MotilityColonic contractions shifted from sporadic, iso-

lated, 1 to 4 contractions per minute (cpm) to reg-ular, propagated, 4 to 9 cpm in 6 of 10 volunteersrecorded with a solid-state transducer during a 1-hour run on a treadmill at 70 to 80% maximumheart rate. Five of the volunteers had previouslyexperienced runner’s diarrhoea.[149] The rise incolonic activity may have accounted for the symp-toms. In the fasted dog, exercise decreased the fre-quency of colonic migrating motor complexes(MMCs), but had no effect on the total or meanduration, or the cycle length of contractile states.In the fed dog, exercise disrupted MMCs andincreased the total duration of contractions thatwere organised as nonmigrating motor complexes.Exercise, in both fasted and fed states, inducedgiant migrating contractions, defecation and massmovements.[150]

2.7 Psychological Factors

Stress-related GI dysfunction has been postu-lated since the beginning of the century.[151] Stressdelays orocaecal transit[152] and inhibits fastingMMCs in the small bowel,[153,154] but increasesmyoelectrical[155] and colonic activity,[156] acceler-ating transit time in humans and experimental ani-mals.[157]

Many athletes experiencing GI symptoms believethat they are aggravated by ‘nerves’ and anxi-ety.[9,10] Up to 57% of athletes with runner’s diar-rhoea complain of GI symptoms before competi-tions; of these, 32% had similar symptoms whenemotionally distressed.[4]

The interaction between the brain and the guthas received much attention in the past few dec-ades. It has been observed that stress-induced GIsecretory and motor responses are mediated by en-dogenous release of corticorelin (corticotropin-releasing factor)[158,159] among others. During ex-ercise, plasma cortisol is increased, but this findingalso occurs in other sports such as cycling.[99]

Table III. Effect of physical exercise on whole-gut transit time

Population Diet Exercise Method Transit time Reference9M active71.5y

Controlsa Inactivity × 2wk 20 ROM × 3 daysAx-ray on fourth day

Delayed 142

14 (8M, 6F): 3groups (A, B and C)28y

Supervised Group A: Jogging 1h/day × 9wkGroup B: Light exercise (<50%V.O2max)

2.5-3h/day × 6wk free diet 0.5h/day × 3wkGroup C: 30-40 min/day light exercise(<50% V

.O2max) × 7wk

10 ROM3 times dailyStool x-ray

UnchangedUnchanged

Unchanged

143

10M sedentary35y

Constanta Walk: 4.5 km/h × 3 daysmax HR 109 beats/min

ROM × 3 daysAx-ray on fourth day

Unchanged 144

20M Specific diet 3 days’ pause3 days’ moderate activity

20 ROM Unchanged 145

10 (6M, 4F)30y

Measured onfourth daya

Rest/cycle/run × 1h/day × 1wk66% max HR50% V

.O2max

50 ROM, MTT-SStool x-ray

Accelerated 146

11M soccer players,9M sedentary

Constanta Soccer training/inactivity 10 ROM × 8 daysAx-ray on ninth day

Unchanged 147

a No specific dietary supervision.Ax-ray = abdominal x-ray; F = female; M = male; max HR = maximum heart rate; MTT-S = mean transit time given single doses of ROM;ROM = radiopaque markers; V

.O2max = maximal oxygen consumption; y = mean age in years.

372 Gil et al.


measurements have not yet been made on athleteswith GI symptoms.

2.6.2 Colonic MotilityColonic contractions shifted from sporadic, iso-

lated, 1 to 4 contractions per minute (cpm) to reg-ular, propagated, 4 to 9 cpm in 6 of 10 volunteersrecorded with a solid-state transducer during a 1-hour run on a treadmill at 70 to 80% maximumheart rate. Five of the volunteers had previouslyexperienced runner’s diarrhoea.[149] The rise incolonic activity may have accounted for the symp-toms. In the fasted dog, exercise decreased the fre-quency of colonic migrating motor complexes(MMCs), but had no effect on the total or meanduration, or the cycle length of contractile states.In the fed dog, exercise disrupted MMCs andincreased the total duration of contractions thatwere organised as nonmigrating motor complexes.Exercise, in both fasted and fed states, inducedgiant migrating contractions, defecation and massmovements.[150]

2.7 Psychological Factors

Stress-related GI dysfunction has been postu-lated since the beginning of the century.[151] Stressdelays orocaecal transit[152] and inhibits fastingMMCs in the small bowel,[153,154] but increasesmyoelectrical[155] and colonic activity,[156] acceler-ating transit time in humans and experimental ani-mals.[157]

Many athletes experiencing GI symptoms believethat they are aggravated by ‘nerves’ and anxi-ety.[9,10] Up to 57% of athletes with runner’s diar-rhoea complain of GI symptoms before competi-tions; of these, 32% had similar symptoms whenemotionally distressed.[4]

The interaction between the brain and the guthas received much attention in the past few dec-ades. It has been observed that stress-induced GIsecretory and motor responses are mediated by en-dogenous release of corticorelin (corticotropin-releasing factor)[158,159] among others. During ex-ercise, plasma cortisol is increased, but this findingalso occurs in other sports such as cycling.[99]

Table III. Effect of physical exercise on whole-gut transit time

Population Diet Exercise Method Transit time Reference9M active71.5y

Controlsa Inactivity × 2wk 20 ROM × 3 daysAx-ray on fourth day

Delayed 142

14 (8M, 6F): 3groups (A, B and C)28y

Supervised Group A: Jogging 1h/day × 9wkGroup B: Light exercise (<50%V.O2max)

2.5-3h/day × 6wk free diet 0.5h/day × 3wkGroup C: 30-40 min/day light exercise(<50% V

.O2max) × 7wk

10 ROM3 times dailyStool x-ray

Unchanged 143

10M sedentary35y

Constanta Walk: 4.5 km/h × 3 daysmax HR 109 beats/min

ROM × 3 daysAx-ray on fourth day

Unchanged 144

20M Specific diet 3 days’ pause3 days’ moderate activity

20 ROM Unchanged 145

10 (6M, 4F)30y

Measured onfourth daya

Rest/cycle/run × 1h/day × 1wk66% max HR50% V

.O2max

50 ROM, MTT-SStool x-ray

Accelerated 146

11M soccer players,9M sedentary

Constanta Soccer training/inactivity 10 ROM × 8 daysAx-ray on ninth day

Unchanged 147

a No specific dietary supervision.Ax-ray = abdominal x-ray; F = female; M = male; max HR = maximum heart rate; MTT-S = mean transit time given single doses of ROM;ROM = radiopaque markers; V

.O2max = maximal oxygen consumption; y = mean age in years.

372 Gil et al.


Pre-competition diarrhoea may be a result ofincreased colonic function due to stress. However,it is questionable whether stress causes GI symp-toms during habitual training sessions.

2.8 Diet

Athletes in general ingest higher amounts ofcarbohydrates and fibre than the sedentary popula-tion.[160] Dietary fibre increases faecal bulk, co-lonic filling, bacterial growth and metabolism inthe colon, thus decreasing transit time and increas-ing the frequency and volume of defecation.

This is supported by the findings of Binghamand Cummings,[143] who stated that when diet isconstant, exercise has no effect on intestinal func-tion.

On the other hand, physically more active peo-ple have higher caloric intakes. Resting orocaecaltransit is faster in high caloric consumers inde-pendently of the composition of the diet.[161]

However, there appears to be no relationshipbetween diarrhoea and dietary fibre or milk in ath-letes with symptoms.[4,10]

2.9 Miscellaneous

2.9.1 InfectionsSwain[162] described a case report of a runner

experiencing ‘typical’ symptoms of runners’ diar-rhoea with urgency, cramps, loose stools and stoolguaiac positive. After extensive tests, stool micro-biology showed Entamoeba histolytica. The pa-tient was treated with antibiotics and the symptomsresolved. Other infections such as Giardia mayalso give similar symptoms.[12] There is a paucityof data in the literature regarding infection, andconclusions must remain speculative.

2.9.2 Ascorbic AcidIt is well known that sportsmen and women

ingest high, and sometimes exceedingly high,amounts of vitamins and mineral supplements.Large amounts of ascorbic acid (vitamin C) maybe the source of GI complaints.[163] However, againno data are available.

2.9.3 Lactose Intolerance and Irritable Bowel SyndromeA survey showed that nervous diarrhoea before

competition was more common in runners who hadsymptoms of lactose intolerance, but there was norelationship with symptoms during or after run-ning.[9]

The same study reported that irritable bowel–like symptoms were related to the need to stop fora bowel motion while training. Irritable bowel syn-drome was found in 14% of runners, a number sim-ilar to that in other population surveys.[9]

2.9.4 DehydrationDehydration is not uncommon during long

training sessions, when runners avoid ingestingfluid due to the difficulties of drinking while run-ning and the unpleasant sensation of a full stomach.Dehydration reduces blood volume, thus aggravat-ing the reduced blood flow to the GI tract that oc-curs during exercise.

Rehrer et al.[71] found that 3.5 to 4% of body-weight loss was associated with an increased inci-dence of GI symptoms during exercise.

3. Conclusions

The effect of exercise on human physiology hasreceived much attention for the past few decades,but the GI tract has often been overlooked. Run-ning produces a variety of GI symptoms in a widenumber of individuals, affecting performance and,in the more severe cases, causing GI ischaemiawith blood loss and anaemia. Studies are neededin order to evaluate the incidence of such disordersin other modes of physical activity.

Figure 1 shows the different hypotheses on theaetiology of running-related GI symptoms. It ismost likely that an interaction of different mecha-nisms affects colonic motility, thus producing GIdysfunction. The mechanical action of runningmust be involved. Reduction of SBF has widelybeen hypothesised as the main factor; however,how severely this occurs is questionable. PG andother GI hormones are also probably involved.How other functions of the GI tract, such as absorp-



tion and permeability, respond to exercise remainsspeculative.

Clearly, the finishing line is still far away, andmore extensive research into the subject is war-ranted to improve our understanding of such a com-mon symptom.

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Running

Increased or decreased colonic motility

GI symptoms

↓GI absorption

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prostaglandins

Stress

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↓Blood flow

↓

↓

Fig. 1. Potential aetiological factors of running-associated gastointestinal symptoms. GI = gastrointestinal; IBS = irritable bowelsyndrome; ↓ = decreased; ↑ = increased.

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Aetiology of Running-Related Gastrointestinal Dysfunction

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