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Lower Gastrointestinal Distress in Endurance Athletes

Ho, Garry W.K.

Current Sports Medicine Reports: March-April 2009 - Volume 8 - Issue 2 - p 85-91
doi: 10.1249/JSR.0b013e31819d6b7b
Abdominal Conditions: Section Articles
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Training regimens and race days place significant demands upon both the competitive endurance athlete and the frequent-recreational runner. Lower gastrointestinal derangements, especially those involving diarrhea and rectal bleeding, are common and can impact adversely both the performance and the health of the athlete. While most cases are relatively benign, more significant and severe symptoms may not only impair sports performance, but also signify more serious disease. The sports medicine clinician should be familiar with the management of these problems in order to optimize treatment, facilitate return to play, and maximize the athlete's potential.

Broadlands Family Practice and Sports Medicine, Ashburn, VA; VCU - Fairfax Family Practice Family Medicine Residency and VCU - Fairfax Family Practice Sports Medicine Fellowship, Fairfax, VA

Address for correspondence: Garry W.K. Ho, M.D., CAQSM Assistant Program Director, VCU - Fairfax Family Practice Sports Medicine Fellowship, 3650 Joseph Siewick Drive, Suite #400, Fairfax, VA 22033 (E-mail: gho@ffpcs.com).

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INTRODUCTION

In the United States, there exists a paradox between the increasing incidence of obesity and the rising numbers of people participating in endurance sports. In recent years, competitive endurance activities have become increasingly popular, and there is little indication of this trend reversing in the near future. The 2007 New York City Marathon saw 39,265 runners participating, as compared with 29,930 runners in 2000 (7). Enthusiast publications, cycling retailers, and specialty running stores continue to grow in numbers, along with sports medicine physician encounters with endurance athletes.

Training regimens and race days place significant demands upon both the competitive endurance athlete and the frequent recreational runner. While the cardiopulmonary and musculoskeletal stresses of endurance activities are obvious and relatively well studied, gastrointestinal complaints are far less well understood but continue to be a significant problem for these athletes. Lower gastrointestinal problems - especially those involving diarrhea and rectal bleeding - are common and can adversely impact both the performance and the health of the athlete. When more significant, diarrhea may contribute to dehydration, heat injury, rhabdomyolysis, and acute tubular necrosis (4). Bloody stools may result in anemia, or may even be a sign of a life-threatening condition, such as an acute intestinal infarction. It is therefore incumbent upon the sports medicine clinician to be familiar with the presentation and management of such complaints in the endurance athlete.

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EPIDEMIOLOGY

A search of the current literature shows that much less is written about diarrhea and rectal bleeding than other ailments encountered by endurance athletes. Still, lower gastrointestinal symptoms are common, occurring more frequently in endurance athletes than other athletes (18). Additionally, the number of publications about Runner's Diarrhea exceeds those regarding other lower gastrointestinal derangements. A study comparing collegiate athletes found that lower gastrointestinal complaints were more common in swimmers than in wrestlers or gymnasts (18). In another study, up to 61% of endurance athletes reported lower gastrointestinal symptoms (22). A survey of marathon runners found that up to 26% reported diarrhea, and up to 54% reported fecal urgency. These symptoms and the need to defecate frequently interrupted their training session or race, and the severity of the complaint was directly proportional to their training mileage or the degree of training intensity. Additionally, women were affected more frequently than men (9,22).

Studies on post-race rectal bleeding have found that 27% of recreational triathletes, 20% of marathon runners, and 87% of 100-mile ultramarathoners tested positive for occult stool blood (1,10,21). Overt hematochezia was reported in 6% of runners after completing a marathon (10). Undoubtedly, the gut is an important athletic organ, which is affected by, and in turn has an effect upon, endurance sporting activity.

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SPORTS SPECIFIC PATHOPHYSIOLOGY

There are many potential pathophysiologic factors that affect the function of the lower gastrointestinal tract in the endurance athlete, potentially contributing to or complicating so-called "Runner's Diarrhea."

Mental stress, vigorous exertion, hyperthermia, dehydration, hypoglycemia, and the relative fatigue of exercise can all increase sympathetic nervous system activity. This, in turn, shifts blood flow away from the viscera and in favor of supplying the working muscles. Exercising at 70% of maximal oxygen consumption (V˙O2max) reduces blood flow to the gastrointestinal tract by 60%-70%; more intense exercise may cause reductions in excess of 80% (1). In isolation, this decrease in splanchnic blood flow is generally well tolerated, since the gut can withstand a 75% reduction in blood flow for 12 h without any major histological changes (2). However, as exercise intensity increases, splanchnic blood flow decreases proportionally (17). This worsening ischemia may then manifest as intestinal mucosal dysfunction - as in colonic malabsorption - or as cellular injury, necrosis, and erosions - contributing to hematochezia. Gut ischemia also may increase membrane permeability, which initiates a cascade of immune-mediated and inflammatory events that cause further injury and impairment to the intestinal mucosa (5). If the ischemia is particularly severe and prolonged, more damaging and irreversible injury may ensue, with varying amounts of necrosis. The resulting ischemic bowel disease may even be acutely life threatening, such as in acute arterial mesenteric infarction - where inflammation is coupled with thrombotic activation (11).

Dehydration may exacerbate gut ischemia and gastrointestinal blood losses. In one study, 80% of runners who lost at least 4% of their body weight from fluid losses during exercise experienced lower gastrointestinal symptoms (16). The complex fluid and electrolyte shifts encountered in endurance exercise also may cause significant intracellular electrolyte imbalances, which then lead to colonic smooth muscle and mucosal irritation (9).

In addition to decreasing splanchnic blood flow, increased sympathetic activity also suppresses the parasympathetic effect upon colonic motility. This decrease in gut tone and resistance accelerates the transit of colonic contents and its passage into the rectum (15), increasing the urge to defecate. Sympathetic nervous system output also may trigger the secretion of gastroenteropancreatic hormones, such as gastrin and motilin, which may directly contribute to diarrhea during higher intensity exercise (19).

Postural factors and mechanical impulse forces transmitted to the viscera also have been proposed to play a role in gastrointestinal fluid and blood losses in endurance athletes (13). The forward-oriented position of cyclists may increase intra-abdominal pressure. Interestingly, gastrointestinal bleeding is relatively infrequent in bicycling compared with the higher-impact, more "up and down" activity of running (16).

Additionally, nutritional factors may play a role, especially foods that increase stool water content. Sports drinks and gels with carbohydrate concentrations in excess of 7%-10% can cause diarrhea and fecal urgency. This so-called "dumping syndrome" stems from an osmotic gradient created across the mucosal semipermeable membrane by the increased luminal carbohydrates. The resulting osmotic shift increases the colonic water content leading to diarrhea. Dietary intake of high glycemic index and high-fiber foods may have a similar effect (16). However, there is considerable variability in glycemic tolerance among athletes, and many are able to adapt to higher carbohydrate loads. Caffeine also may act as a laxative and should be avoided during higher intensity endurance exercise (14).

Medications and ergogenic aids also may play a role, and it is important to consider these in any athlete complaining of gastrointestinal symptoms. The inappropriate use of nonsteroidal anti-inflammatory drugs (NSAIDs) has been proposed to contribute to gastrointestinal bleeding in endurance athletes, but the role that NSAIDs actually play remains uncertain. Although NSAID misuse has been associated with gastritis and peptic ulcer disease, studies have yet to show a direct correlation between NSAIDs and gastrointestinal bleeding in endurance athletes (1).

In addition to the above sports-specific factors, it is important to include causes of diarrhea and rectal bleeding that are prevalent in the general population as well. Perianal disease - such as hemorrhoids, fissures, fistulae, and chafing - inflammatory bowel diseases, malabsorption syndromes, pancreatic disease, irritable bowel syndrome, pseudomembranous colitis, Traveler's diarrhea, and other infectious causes should all be considered as well (8). The specific pathophysiology of these conditions is discussed elsewhere (6,8,23).

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DIAGNOSIS

The differential diagnosis for diarrhea and rectal bleeding in the endurance athlete can be quite long (Table 1). One possible approach is to divide patient-athletes into an under-40 (yr old) and an over-40 group (20). In the younger group, malabsorption syndromes, infections, inflammatory bowel disease, Runner's Diarrhea, and other functional impairments are the most likely causes of complaint. In the older group, concerns such as colon cancer, pancreatic disease, and diverticular disease also should be considered. A proposed clinical algorithm is presented here (Figure). Additionally, while Runner's Diarrhea - also known as Runner's Trots (4) - is a common diagnosis, it is a clinical one and a diagnosis of exclusion.

TABLE 1

TABLE 1

Figure. C

Figure. C

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History

Obtaining an accurate, reliable, and comprehensive history from the patient-athlete can be challenging. Endurance athletes are often reluctant to discuss issues surrounding lower gastrointestinal complaints due to fear of embarrassment, or an assumption that their symptoms are untreatable, expected, or "just part of the sport." Nevertheless, it is essential to be direct, patient, understanding, and detailed while taking the history.

The sports medicine clinician should ask about the nature of the diarrhea or rectal bleeding - including the onset, amount, duration, frequency, color, and consistency of bowel movements. A persistent decrease in stool caliber, so-called "pencil-like stools," may be a sign of a colonic neoplasm, and a colonoscopy should be considered in these cases. Be careful to differentiate between melena and hematochezia. Intermittent rectal bleeding can predispose athletes to anemia, while more persistently bloody diarrhea may be a sign of ischemic bowel disease, especially when it occurs with acute abdominal pain (12). It also is important to ask the patient when the symptoms appear in relation to exercise, meals, and time of day. Ask about associated symptoms, such as abdominal pain - including the location of the pain - cramping, bloating, nausea, vomiting, hematemesis, and intermittent constipation. Constitutional symptoms also may be significant, such as fever, chills, malaise, unexpected fatigue, dizziness, weight loss, or other systemic complaints. Since inflammatory bowel diseases (IBD) also may affect the musculoskeletal system, lungs, skin, eyes, and kidneys, ask the patient about any extraintestinal symptoms of inflammatory bowel disease (23). Exacerbating and alleviating factors provide helpful clues as well. Abdominal cramping relieved by defecation and worsened by stressors may indicate irritable bowel syndrome (6).

An inventory of the patient's dietary, herbal, and supplement intake is imperative, including the use of sports drinks, sports gels, caffeine, alcohol, tobacco, and dietary fiber (Table 1). A food diary is often helpful, since patients may have difficulty recalling specific details about their dietary intake. If needed, a dietician or nutritionist may be consulted.

Obtaining a medication history and past history of known medical conditions also is essential. Many preexisting conditions, such as inflammatory bowel disease, can be exacerbated by higher intensity exercise. The timing of any dietary or medication intake in relation to the athlete's symptoms also may provide vital clues. A travel history may reveal exposures to infectious causes.

Training habits play a key role in many complaints from endurance athletes. Recent changes in the athlete's training regimen, intensity, duration, or distance may be significant, especially if symptoms tend to worsen proportionally with increasing exertion. Ask the athlete how the diarrhea, rectal bleeding, or associated symptoms have impacted training or competition performance. Review of a training diary often is helpful.

A family history of diseases - such as inflammatory bowel disease, colon cancer, and irritable bowel syndrome - may place the patient at a higher risk for these conditions. A concise psychosocial assessment also should be performed, with particular attention given to the athlete's stress and anxiety levels both during exercise and in daily living.

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Physical Examination

The physical examination may be helpful, but is often nonspecific. Nonetheless, a careful examination should be performed. Look for fever and cardiopulmonary abnormalities in the vital signs. Orthostatic blood pressure and heart rate measurements may point to dehydration or anemia. An abdominal examination for localized tenderness, peritoneal signs, palpable masses, and bowel sounds is essential. A rectal examination with stool guaiac for occult blood also should be done. Additionally clinicians should look for findings consistent with systemic diseases, such as hyperthyroidism or the extraintestinal manifestations of inflammatory bowel disease. A more detailed discussion of inflammatory bowel disease in athletes is available elsewhere (23).

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Diagnostic Tests and Studies

A number of laboratory and diagnostic studies may be considered in the evaluation of diarrhea or rectal bleeding in the endurance athlete. A complete blood count and metabolic chemistry panel will help uncover associated problems such as anemia, an elevated white blood cell count due to infection, hypokalemia, and other electrolyte disturbances. Anemia may then prompt the clinician to search for iron deficiency - including serum iron, total iron biding capacity, and ferritin levels - since this is often present in endurance athletes. A hepatic panel to include transaminases and bilirubin, amylase, and lipase levels are useful for excluding hepatitis, biliary tract disease, and pancreatic disease. Since hyperthyroidism may be a cause of diarrhea, a thyroid stimulating hormone (TSH) level also may be helpful. An elevated erythrocyte sedimentation rate (ESR) and C-reactive protein (CRP) are often seen in inflammatory bowel disease and may be indicated - along with a colonoscopy with biopsies - based upon the patient's past medical and family history (23).

Potential food intolerances and allergies can be further evaluated with a number of tests. Laboratory tests for gluten-sensitive enteropathy (Celiac sprue) include anti-gliadin antibody titers - both immunoglobulin (Ig) G and IgA - and a tissue transglutaminase antibody assay. If lactose intolerance is suspected, a trial of over-the-counter lactase tablets or avoidance may be more practical than a hydrogen breath test. A number of laboratory assays are available for food allergies as well.

Stool studies are often included in the diagnostic assessment of the athlete with diarrhea. Indications for stool studies include gross hematochezia, profuse diarrhea with dehydration, persistent diarrhea for more than 48 h, constitutional signs such as fever, severe abdominal cramping, recent travel, or possible exposure to infectious diarrheal agents, and in cases where initial treatment fails or no other identifiable cause can be found. Stool studies also should be considered in the immunocompromised or older athlete. Laboratory examinations of stool specimens include fecal leukocyte count and bacterial stool culture for Salmonella, Shigella, Yersinia, and Campylobacter species, as well as certain strains of Escherichia coli. Stool specimens also should be examined for ova and parasites. Antigen assays for Giardia, Entaemoeba histolytica, and Clostridium difficile toxin also are important, especially in the traveling athlete or in the context of recent antibiotic use. If a malabsorption syndrome is suspected, quantitative assays for fecal fat, protein, and reducing substances may be helpful.

For athletes with persistently positive fecal occult blood, bloody diarrhea, failure to improve with treatment, or when no other identifiable cause can be found, referral for gastroenterology consultation, colonoscopy, and possibly esophagogastroduodenoscopy should be considered. Colonoscopy is indicated if inflammatory bowel disease or irritable bowel syndrome are suspected. Additionally, endoscopic evaluation is especially important in patient-athletes 50 yr of age or older, because the risk of malignancy is higher for these individuals.

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Ischemic Bowel Diseases

Of particular note are the ischemic bowel disease entities, in part because they can be life threatening, and in part because they may be easily missed unless the sports medicine clinician maintains a high index of suspicion and is prepared to obtain the appropriate diagnostic studies. There are four distinct syndromes of ischemic bowel disease: acute arterial mesenteric infarction, chronic arterial mesenteric ischemia, mesenteric venous thrombosis, and colonic ischemia (11).

Acute arterial mesenteric infarction (AAMI) presents with acute fever, tachycardia, bloody stools, and severe abdominal pain - often described as pain out of proportion to the physical examination, with or without peritoneal signs. Acute small intestine or ascending colon ischemia or infarction occurs due to thrombosis, emboli, or sustained severe splanchnic ischemia. A high index of suspicion is required since severe cases may be catastrophic with mortality rates higher than 80%, prompting abdominal CT scan, mesenteric angiography, or even exploratory laparotomy (11).

Chronic arterial mesenteric ischemia - also known as intestinal angina - presents with more mild, recurrent abdominal pain, functional bowel derangements, and weight loss. Symptoms are generally more prominent with exercise and with meals, due to increased tissue demand in the context of a fixed arterial stenosis (11).

Mesenteric venous thrombosis may be acute, subacute, or chronic, but usually is more indolent than AAMI. Symptoms include nausea, vomiting, rectal bleeding, and abdominal pain out of proportion to examination findings. Risk factors include hypercoagulable states, portal hypertension, abdominal inflammatory states, and trauma. If this syndrome is suspected, an abdominal CT scan is important because the ischemia may progress to infarction (11).

Colonic ischemia is the most common form of ischemic bowel disease, presenting as crampy lower left quadrant pain, and bowel movements consisting of blood mixed with stool. Colonoscopy should be done within the first 24-48 h of rectal bleeding, since findings often resolve rapidly, with completely normal results after 1 wk being typical (11).

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TREATMENT

The successful therapeutic management of the endurance athlete with diarrhea or rectal bleeding depends upon an accurate diagnosis. However, given the vast number of diagnostic studies that can be obtained on a myriad of potential culprits, a therapeutic trial may be considered as part of the diagnostic process. Nonetheless, any treatment should address an underlying gastrointestinal disease, identifiable causes, or associated sequelae uncovered during the diagnostic process, whenever possible (Figure). Detailed discussion for the treatment of the distinct gastrointestinal disease entities in Table 1 is beyond the scope of our review, but is available elsewhere (6,8,23).

However, the treatment of inflammatory bowel disease in the endurance athlete is worth noting here, since there may be extraintestinal manifestations that are particularly important in active individuals. Medical treatment for inflammatory bowel disease includes aminosalicylates, corticosteroids, immunomodulating agents, methotrexate, and cyclosporin (23). Patients with inflammatory bowel disease are also at increased risk for osteopenia, osteoporosis, and stress fractures, and should be sure to receive adequate calcium and vitamin D supplementation, abstain from tobacco use, avoid excessive alcohol use, and may need baseline and follow-up bone density measurements. Monitoring for arthritic symptoms is also important. Pulmonary manifestations may require the use of inhaled corticosteroids and bronchodilators, and the athlete with inflammatory bowel disease should be screened for anemia. Most of these extraintestinal manifestations will benefit from optimal treatment of inflammatory bowel disease, in collaboration with a qualified gastroenterologist (23). Additionally, these athletes should avoid strenuous exercise whenever their disease is active, gradually returning to training when symptoms from an exacerbation have resolved.

If the patient athlete is afebrile with normal vital signs, and no other discrete gastrointestinal disease is suspected from the diagnostic process, Runner's Diarrhea may be assumed as a diagnosis of exclusion. The general approach to treating Runner's Diarrhea is to control any risk factors, and to allow for the gut to adjust and adapt to the demands of training and competition. Studies have shown that splanchnic blood flow is enhanced in trained athletes compared with less fit individuals. The resolution of many lower gastrointestinal symptoms also has been demonstrated with adequate training, compared with untrained states (12).

The initial treatment step for Runner's Diarrhea is to reduce the training intensity, duration, and distance for 1-2 wk and observe for resolution of symptoms (3). Those with bloody diarrhea with no identifiable cause should cease running until all symptoms abate. Once the patient is asymptomatic, a cross-training regimen with lower-impact activities - such as cycling, swimming, or rowing - may be implemented to maintain cardiopulmonary fitness. Running may then be titrated back gradually into the training regimen. The athlete also should be advised to avoid NSAIDs, aspirin, antibiotics, and caffeine (12). Dietary discretion - including a low-residue, low-fiber diet and avoidance of sports drinks and gels with carbohydrate concentrations greater than 7%-10% - should be recommended (12). Maintenance of adequate hydration is paramount for all endurance athletes, particularly those with lower gastrointestinal symptoms, and especially during training and competition.

A number of medications have been used in the treatment of Runner's Diarrhea. However, many antidiarrheals and antimotility medications may be problematic, given their negative anticholinergic effects on sweating and thermoregulation. This may predispose some athletes to heat illness. Opiate and atropine based preparations should also be avoided. Nonetheless, loperamide - taken at over-the-counter doses prior to exercise - may be considered in more severe cases of non-bloody diarrhea that place the athlete at significant risk for dehydration, heat intolerance, and electrolyte derangements. Antispasmotics for abdominal cramping, especially if irritable bowel syndrome is suspected, may be considered as well. However the risk of anticholinergic effects with these drugs also should be considered. Finally, histamine H2 receptor antagonists and proton pump inhibitors may be effective in athletes with bloody diarrhea caused by hemorrhagic gastritis (1).

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RETURN-TO-ACTIVITY AND PREVENTION

Once the patient-athlete is completely asymptomatic at rest and with lower-to-moderate intensity aerobic cross-training, regular training activities may then be re-introduced, monitoring for symptom recurrence. If symptoms recur despite adequate rest and gradual titration of activity, further evaluation for an unidentified underlying cause should be pursued.

As the athlete begins to increase his or her exercise intensity, duration, or mileage, a prevention strategy should be encouraged (Table 2). Dietary measures such as a low-residue, low-fiber diet for the 2-3 d leading up to a longer, higher-intensity training session or competition, as well as avoidance of sports drinks and gels with higher carbohydrate concentrations, should be continued. Athletes also should include any nutritional, supplement, and hydration strategies they will use in competition in their training regimens; new and previously untested products should not be used by the athlete on race day if he or she has not tried these during training. Environmental acclimatization measures also should be considered in any endurance training program. Finally, ensuring that increases in training intensity or duration are gradual, allowing adequate active rest between training sessions, will allow the gut to adapt to the increased training load.

TABLE 2

TABLE 2

Should an athlete be at risk for infectious diarrhea - particularly in the traveling athlete - he or she should be advised to observe infection control measures, such as frequent hand washing, eating only adequately cooked food, not eating unwashed fruits and vegetables, and only drinking bottled or purified water. A more detailed discussion on chemoprophylaxis in Traveler's diarrhea is available elsewhere (8).

Athletes who have been found to have a discrete gastrointestinal disease, such as inflammatory bowel disease, should be advised to abstain from strenuous exercise whenever their disease is active, especially when there is bloody diarrhea (20,23). All athletes who have had diarrhea or rectal bleeding also should be educated on the warning signs of hemodynamic compromise and anemia, such as dizziness, unexpected fatigue, dyspnea, or an unexpectedly elevated heart rate. Once the athlete has resumed a training regimen and chosen activities, it is also important that he or she continue to monitor for any change in gastrointestinal symptoms, as this may indicate a new, different diagnosis as opposed to persistent irritable bowel syndrome or Runner's Diarrhea.

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CONCLUSION

Lower gastrointestinal symptoms such as diarrhea, rectal bleeding, and the untimely urge to defecate are common issues that afflict endurance athletes. While most cases are relatively benign and mostly inconvenient, more significant and severe symptoms not only may affect adversely sports performance, but also signify more serious disease. The sports medicine clinician should be familiar with the management of these problems in order to optimize treatment, facilitate return to play, and maximize the athlete's potential.

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References

1. Baska RS, Moses FM, Deuster PA. Cimetidine reduces running-associated gastrointestinal bleeding. A prospective observation. Dig. Dis. Sci. 1990; 35:956-60.
2. Boley SJ, Brandt LJ, Frank MS. Severe lower intestinal bleeding: diagnosis and treatment. Clin. Gastroenterol. 1981; 10:65.
3. Brouns F, Beckers E. Is the gut an athletic organ? Sports. Med. 1993;15:242-57.
4. Fogoros R. Runner's trots. Gastrointestinal disturbances in runners. JAMA. 1980; 243:1743-4.
5. Gisolfi CV. Is the GI system built for exercise? News Physiol. Sci. 2000; 15:114-9.
6. Heiman DL, Lishnak DL, Trojian TH. Irritable bowel syndrome in athletes and exercise. Curr. Sport Med. Rep. 2008; 7(2):100-3.
7. ING New York City Marathon - Complete Marathon Results Archive. Available at: http://www.ingnycmarathon.org/results/index.php. Accessed October 2008.
8. Karageanes SJ. Gastrointestinal infections in the athlete. Clin. Sports Med. 2007; 26:433-48.
9. Keeffe EB, Lowe DK, Goss JR, Wayne R. Gastrointestinal symptoms of marathon runners. West. J. Med. 1984; 141:481-4.
10. McCabe ME, Peura DA, Kadakia SC, Bocek Z, Johnson LF. Gastrointestinal blood loss associated with running a marathon. Dig. Dis. Sci. 1986; 31:1229-32.
11. Moses FM. Exercise-associated intestinal ischemia. Curr. Sports Med. Rep. 2005; 4:91-5.
12. Murray R. Training the gut for competition. Curr. Sports Med. Rep. 2006; 5:161-4.
13. Porter AM. Marathon running and the caecal slap syndrome. Br. J. Sports Med. 1982; 16:178.
14. Putukian M, Potera C. Don't miss gastrointestinal disorders in athletes. Phys. Sportsmed. Available at: http://www.physsportsmed.com/issues/1997/11nov/putukian.htm. Accessed October 2008.
15. Rao SSC, Beaty J, Chamberlain M, et al. Effects of acute graded exercise on human colonic motility. Am. J. Physiol. (Gastrointest. Liver Physiol.) 1999; 276:G1221-6.
16. Rehrer NJ, Janssen GM, Brouns F, et al. Fluid intake and gastrointestinal problems in runners competing in a 25-km race and a marathon. Int. J. Sports Med. 1989;10(suppl 1):S22-5.
17. Sawka MN, Young AJ. Physiological systems and their responses to conditions of heat and cold. In: Tipton CM, Sawka MN, Tate CA, Terjung RL, editors. ACSM's Advanced Exercise Physiology, Philadelphia: Lippincott Williams & Wilkins; 2005. pp. 535-63.
18. Strauss RH, Lanese RR, Leizman DJ. Illness and absence among wrestlers, swimmers, and gymnasts at a large university. Am. J. Sports Med. 1988; 16(6):653-5.
19. Sullivan SN, Champion MC, Christofides ND, Adrian TE, Bloom SR. Gastrointestinal regulatory peptide responses in long-distance runners. Phys. Sportsmed. 1984; 12(7):77-82.
20. Swain RA. Exercise-induced diarrhea: when to wonder. Med. Sci. Sports Exerc. 1994; 26(5):523-6.
21. Worme JD, Doubt TJ, Singh A, et al. Dietary patterns, gastrointestinal complaints, and nutrition knowledge of recreational triathletes. Am. J. Clin. Nutr. 1990; 51(4):690-7.
22. Worobetz LJ, Gerrard DF. Gastrointestinal symptoms during exercise in Enduro athletes: prevalence and speculations on the aetiology. N.Z. Med. J. 1985; 98(784):644-6.
23. Zakaria AA, Rifat SF. Inflammatory bowel disease: concerns for the athlete. Curr. Sports Med. Rev. 2008; 7(2):104-7.
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