Complaints of abdominal pain and other gastrointestinal (GI) symptoms are relatively common among athletes. These problems may interfere with athletic activities and produce dramatic examples of unexpected illness and disability. Ischemic bowel disease may present with a variety of characteristic clinical syndromes that range from acute abdominal catastrophe to GI bleeding to recurrent abdominal pain. Health professionals caring for athletes and active people with underlying medical conditions need to have a thorough understanding of ischemic bowel disease. Over the past few decades the literature on GI disorders associated with exercise has expanded and clinical research in this field is ongoing. However, much remains uncertain and untested. The vast majority of published work has studied normal subjects under submaximal efforts for relatively short durations. There are few data regarding the effect of sustained strenuous exercise or the effects of exercise on patients with underlying GI disorders. This article reviews ischemic bowel disease, the physiology of the mesenteric vascular system during exercise, and the clinical reports of ischemic bowel disease associated with exercise.
The following two cases illustrate a spectrum of ischemic bowel disease associated with exercise.
A 42-year-old man presented with abdominal pain and rectal bleeding after a 6-mile run. On the day of admission he felt well and went for a run with some friends. The running pace was faster than his usual but he kept up with some effort. At 5 miles he began to suffer “crampy” lower quadrant abdominal pain. At 6 miles he had the urge to have a bowel movement. One hour following his run, he developed nausea and three episodes of hematochezia.
He was moderately orthostatic, had right lower quadrant tenderness without mass or guarding, and frank blood in the rectal vault. Nasogastric aspirate revealed clear bile and a sigmoidoscopy showed blood above 60 cm. His hematocrit decreased from 48% to 42%. Other laboratory studies were normal. He was treated with intravenous fluid resuscitation, remained asymptomatic, and underwent an electrolyte purge.
Upper endoscopy the next morning showed only a small nonbleeding gastric erosion. Colonoscopy was normal to the hepatic flexure but showed confluent submucosal hemorrhage and edema to the cecum. The terminal ileum was normal. Biopsies showed intact mucosa with hemorrhage pathologically consistent with ischemic damage. The patient was discharged, remained asymptomatic and resumed recreational jogging within 2 weeks without subsequent recurrence .
A young professional male triathlete and prerace favorite collapsed near the finish of an Ironman triathlon. He had been in excellent condition prior to the race and completed the 3.9-km swim segment with the leaders. During the 180-km bike segment he was unable to keep fluids or nutrition down but managed to stay near the lead group, completing this segment and starting the 42.2-km run. During the run he began to vomit fluids and suffer diarrhea. He collapsed 50 m from the finish line. He was treated with intravenous fluids and released. Because of continued abdominal pain, distention, and fever he underwent endoscopic evaluation leading to laparotomy and right hemicolectomy 24 hours later for gangrenous ischemic colitis. He recovered and returned to successful elite racing over the next few years, but suffered multiple bowel obstructions necessitating exploration and lysis of adhesions .
Ischemic Bowel Disease
Ischemic damage occurs when the tissue is deprived of nutrients and oxygen. Normal bowel can tolerate up to 75% reduction in mesenteric blood flow for up to 12 hours with no change in light microscopy . During brief episodes of ischemia, little bowel damage may be observed endoscopically or histologically. However, functional derangements may occur causing abdominal pain or diarrhea. If adequate blood flow is immediately restored, little if any damage may be observed. However, as the insult lengthens, damage may become apparent microscopically and the injury may still be reversible. If the ischemia is severe enough, damage becomes irreversible and variable degrees of necrosis will ensue. The clinical result will then depend on the severity and location of the insult.
There are four major syndromes of ischemic bowel disease that are classically recognized. Acute arterial mesenteric infarction (AMI) is the most feared of all these syndromes and results from inadequate blood flow to the small intestine and right colon. Clinical manifestations depend upon the extent of injury and the etiologies, which include superior mesenteric artery (SMA) embolus, nonocclusive mesenteric ischemia, SMA thrombosis, and focal segmental ischemia. In severe cases this may lead to an acute abdominal catastrophe with mortality rates above 80% .
Because AMI carries such a severe outcome, a high index of clinical suspicion is required. Patients present with severe abdominal pain, classically stated to be out of proportion to the findings on abdominal examination. There may also be signs of peritoneal inflammation with fever, tachycardia, and bloody stools. Abdominal computed tomography (CT) scan may be helpful in demonstrating injury or thrombosis but mesenteric angiography is the diagnostic procedure of choice. Nonocclusive mesenteric ischemia is documented angiographically and is the most likely associated etiology with exercise in the otherwise healthy athlete. At times the diagnosis is only established at exploratory laparotomy [5••].
Chronic arterial or mesenteric ischemia, also known as intestinal angina, generally presents as a more indolent course with recurrent abdominal pain and functional derangements of the bowel. Fixed arterial stenosis limits blood flow regardless of the tissue demand. The patient may have other manifestations of systemic vascular disease, such as coronary heart disease or peripheral vascular disease. The patients suffer weight loss and abdominal pain when demand for visceral blood flow increases above a threshold value, generally precipitated by a meal.
Mesenteric venous thrombosis may also present as an acute, subacute or chronic condition but is usually a more indolent condition than AMI. The etiologies of this condition are hypercoagulable states, portal hypertension, abdominal inflammatory states, or trauma. The clinical presentation is variable but most patients present with abdominal pain, typically out of proportion to the physical findings. Nausea, vomiting, and lower GI bleeding may also complicate the picture in severe cases. The condition may also progress to bowel infarction. The diagnosis is generally made by abdominal CT scan.
Colonic ischemia is the most common form of intestinal ischemia particularly among the elderly. The clinical presentation can range from reversible hemorrhagic colitis to stricture, gangrene, and fulminant colitis. Ischemic colitis may result from changes in systemic circulation or mesenteric anatomy. The colon is thought to be more sensitive to ischemic changes due to its relatively low blood flow and increased sensitivity to the autonomic nervous system. The causes of this syndrome are multiple but exercise has been implicated. The clinical presentation is crampy lower left quadrant pain and passage of blood mixed with stool. Bleeding is generally limited and often resolves without therapy or transfusion requirements. Most frequently the left colon, including sections from the sigmoid to the splenic flexure (the “watershed” regions), are involved and colonoscopy is the most sensitive method of demonstrating injury. Colonoscopy will typically demonstrate submucosal hemorrhage and edema. Evaluation should be performed within the first 24 to 48 hours as these findings resolve rapidly. Endoscopy after 1 week is typically normal except in severe cases. In some cases resolution may take months. Stricture is a possible outcome but generally is managed conservatively unless symptoms are severe. Resolution of the stricture is possible up to 2 years following the insult [6••]. Angiography is only indicated for severe symptoms suggesting AMI or a diagnosis other than ischemic colitis is considered. Occasionally ischemic colitis limited to the ascending colon may suggest an AMI syndrome. Surgery is required for presentation suggesting infarction, perforation or massive bleeding.
Exercise Physiology Studies
Visceral blood flow may be measured with angiographic studies, Doppler ultrasound vascular analysis or gastric tonometry. Alternatively, blood flow is sometimes estimated using liver blood flow clearance studies with markers such as indocyanine green.
Cardiac output increases during exercise with flow diverted to exercising muscles. Visceral blood flow has been documented to fall by 50% to 80% of baseline values [7,8]. Using Doppler technique of the SMA to study healthy volunteers at rest and up to 30 minutes after completing exercise (15 min walking 5 km/h on a 20% grade in both fasting and following a 390 kcal liquid meal), up to a 43% decrease in SMA flow was noted . Another study used duplex ultrasonography to assess celiac and SMA blood flow with exercise and meals in 19 humans. Submaximal cycling decreased visceral blood flow from 32% to 50% .
Gastrointestinal blood flow and function has been measured indirectly with other methods. Mucosal perfusion was studied in 10 healthy subjects with gastric air tonometry. Two short stages on a cycle ergometer to 80% and 100% of maximum heart rate showed that intragastric-arterial pCO2 increased suggesting gastric ischemia with maximal exercise . Another study using similar technique but a different cycling exercise protocol showed that submaximal cycling lead to early derangement of gastric mucosal energy balance . This technique has been correlated with angiographic findings. A study of 14 patients with unexplained abdominal pain or weight loss was performed. Angiography was normal in seven but showed more than 50% stenosis of the celiac artery or SMA in seven others. Gastric tonometry before and after 10' submaximal exercise was normal in patients with normal angiograms but was abnormal in the remainder and correlated with the degree of stenosis.
It is difficult to measure mesenteric blood flow in the athlete and data are limited in symptomatic individuals. In 41 marathon skiers, 19% developed GI symptoms and 7% were occult blood positive after the race . SMA blood flow was measured by duplex scanning in two trained runners. An asymptomatic runner had insignificant change but a runner treated for anemia showed a 20% to 40% decrease in flow with exercise.
Visceral angiograms are infrequently performed in these cases. Magnetic resonance angiography/MRI was performed in an ischemic colitis case [14•]. Mesenteric angiography was performed as part of an exhaustive evaluation for exercise-associated recurrent GI bleeding in a young female runner [15•]. These tests were normal.
During exercise, particularly during endurance events, the athlete may become hypovolemic. This may be compounded by hyperthermia, dehydration, and potentially by the use of nonsteroidal anti-inflammatory drugs (NSAIDs). GI symptoms have been correlated with dehydration and suggest that ischemia plays a role in these problems. In a group of marathon runners, 80% of those who lost over 4% of their body weight suffered GI symptoms .
During prolonged exercise there is an ongoing need for intestinal function and absorption of fluids, electrolytes, and nutrients to replace lost elements. This ordinarily requires an increase in visceral blood demand that may be inadequate. This can result in an increase in the relative mismatch between visceral supply and demand worsening clinical ischemia. There are few data under these conditions.
Athletes with intestinal ischemia generally present due to complaints of abdominal pain and GI bleeding. Bleeding may be acute upper or lower GI bleeding, chronic bleeding and anemia, or incidentally noted occult (fecal occult blood test [FOBT])-positive stool. Active people with underlying GI disorders may have exacerbations of their disease but data are limited.
The incidence of exercise-associated GI bleeding is uncertain and studies are inconclusive. Examples of acute upper and lower GI bleeding are not common and are generally published as case reports or small case series. The initial report was a medical student with recurrent hematochezia after strenuous running . Two additional cases followed. In one abdominal pain suggested acute appendicitis, led to exploratory surgery with findings of ischemia .
Studies to determine the incidence of GI bleeding with running by means of surveys and prospective studies of FOBT after running events were published. The first study noted that three of 39 marathon runners converted to FOBT positive after the race . A questionnaire survey of runners found a postrace incidence of hematochezia of 1.2% to 1.8% . Other studies found the incidence of postrace FOBT positivity to range from 8% to 85%. Higher values were seen during ultramarathon races [21–24]. Attempts to quantify blood loss in runners have shown a temporal profile of bleeding that peaks 24 to 48 hours following the event [25,26]. Several other publications showed that bleeding is more common after competition than with training suggesting bleeding is related to the degree of effort [27–29].
Endoscopic surveys of runners have been published but are inadequate to determine the incidence of running-associated GI lesions. The first prospective endoscopic trial studied seven of nine runners who converted to FOBT positive following a marathon . Only three were studied within 48 hours. Two had oozing antral erosions and one had hyperemia and erosion of the splenic flexure. Evaluations done 4 to 30 days later were negative. A study of 16 competitive runners after a 20-km race suggested hemorrhagic gastritis (HG) was common. Upper endoscopy was done on all and colonoscopy on those who were FOBT positive. Gastritis was found in 16, esophagitis in six, and a gastric ulcer in one. Colonoscopy was done in four runners. One had multiple erosions of the splenic flexure and one had a polyp .
Hemorrhagic gastritis is the most commonly reported exercise-associated lesion with GI bleeding. HG is transient and generally resolves within 72 hours [32–34]. HG is mediated at least in part by gastric acid. A young woman with recurrent HG was documented by endoscopy to recur with running and resolve with rest. If cimetidine was given to block acid, the gastritis resolved even while running continued [35••]. Histologic changes of gastritis may occur in runners in the absence of obvious endoscopic findings [36,37].
The mechanism of exercise-associated HG is felt to be ischemia mediated by gastric lumenal acid. Prospective trials using cimetidine in runners have not been conclusive. In an initial study cimetidine was found to reduce FOBT positivity conversion following an ultramarathon from 85% to 12.5% . Subsequent double-blinded trials using similar dosages suggested a reduction in bleeding as measured by either FOBT or HemoQuant (Mayo Medical Laboratories, Rochester, MN) but were not statistically significant . No studies have been published with more potent proton pump inhibitors.
The colon has been the second most common location for exercise-associated GI bleeding. Since the initial case , numerous others have described various presentations of presumed ischemic colitis associated with exercise. A 33-year-old runner developed hematochezia after a marathon and a cecal lesion suggestive of ischemia was seen . A runner developed hematochezia after a 10-km high-altitude run and was noted to have HG and colitis with rhabdomyolysis and hematuria . Our own publication of this syndrome is illustrated above . An elite marathoner suffered ischemic sigmoid colitis and was extensively evaluated without other causes [14•]. The amount of effort associated with the finding of ischemic colitis is variable and may occur with relatively nonstrenuous events . Ischemic colitis has been confirmed operatively. A 42-year-old woman presented with hematochezia, vomiting, and progressive abdominal pain 3 days after completing a half-marathon in the heat. At laparotomy bloody ascites and an inflamed transverse and ascending colon were found and a subtotal colectomy performed. Histology demonstrated ischemic colitis .
Intestinal infarction associated with exercise appears to be a rare event. Kam et al.  published a case of a 65-year-old physician and long-time 50 km/wk runner who developed abdominal pain 30 minutes after a 6-km run. The severity of the presentation led to mesenteric angiography showing small bowel hyperemia but no SMA occlusion. A 1-m segment of gangrenous ileum was resected at laparotomy. Doppler interrogation showed good flow to the bowel wall and no venous clots were noted. Interestingly, the patient had a long history of explosive watery diarrhea during jogging. The authors speculate he may have manifested his sensitivity to ischemia with his prior episodes of running-associated diarrhea . Omental infarction and acute pancreatitis have also been associated with running [43,44].
The response of the mesenteric circulation to exercise is complex and athletes may have increased autonomic sensitivity. There is a spectrum of clinical presentations of ischemic bowel disease and, in the athlete, the symptoms may be superimposed on dehydration, hyperthermia, and exhaustion. Physicians should recognize the acute and chronic presentations and the optimum methods of diagnosis and treatment.
Abdominal pain and diarrhea are typical initial symptoms of ischemia and generally limit further damage by inhibiting activity. This may be overridden during extreme athletic competition or other significant endurance events. Athletes and coaches should be aware that continuing sport in the face of progressive abdominal pain, diarrhea or rectal bleeding risks the dangers of ischemic bowel disease.
Although the incidence is unknown, athletes with recurrent symptoms of abdominal pain and diarrhea may be at increased risk for ischemic damage and infarction. Although infrequently studied, no underlying anatomic abnormalities have been noted.
Ischemic gastritis is generally reversible and may be controlled with effective acid blockade. Ischemic colitis generally presents with diarrhea and bleeding. It is usually mild but may require volume and transfusion support, rarely progressing to need for resection or stricture. The athlete is usually able to resume activities without restriction.
Athletic activity may exacerbate the symptoms of underlying GI disorders but has not been well studied. Athletes who develop recurrent abdominal pain, diarrhea or GI bleeding should be evaluated as nonathletes for age-appropriate usual causes of GI disability.
The opinions and assertions contained herein are the private views of the authors and are not to be construed as official or as reflecting the views of the Department of the Army, the Department of Defense, or the United States Government.
References and Recommended Reading
Papers of particular interest, published recently, have been highlighted as: • Of importance, •• Of major importance
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