Gastrointestinal (GI) conditions in athletes and active persons are common and are seen frequently by sports medicine care providers. Despite the myriad benefits that result from high- level physical activity, exercise may place significant stress on the GI tract, which in turn may result in a number of characteristic GI disorders. The appreciation of this relationship is important for both care providers and athletes who must team together to minimize distressing GI symptoms and subsequent impairment in performance. Common GI disorders in athletes may mimic those seen in the general population but also may present as unique entities seen primarily in persons who exercise at a high level. This chapter addresses a number of common entities with a focus on their recognition and appropriate management in athletes.
Frequent, high-intensity exercise may cause a number of undesirable GI symptoms such as heartburn, chest pain, bloating, belching, nausea, vomiting, abdominal cramps, frequent urge to defecate, and diarrhea. These symptoms are reported by approximately 20% to 50% of high-performance athletes and are encountered more commonly in women than in men. They are also more common in younger athletes and in endurance athletes compared with their nonendurance counterparts. Body position and movement also appear to play a role; for example, the forward positioning of cyclists appears to protect them from GI tract issues, as opposed to the higher impact, jostling abdominal movements of runners. Other suggested mechanisms for increased GI distress include a number of neurologic/immunologic/endocrine adaptations to exercise. Increased catecholamines and an increase in several GI peptides including gastrin, motilin, secretin, peptide histidine-methionine, and vasoactive intestinal peptide result in increased gut transit time that negatively affects GI homeostasis.
Gastrointestinal Tract Ischemia
GI tract ischemia as a result of attenuated GI blood flow is a well-defined exercise adaptation that redirects blood flow to active muscles and the pulmonary vasculature. Vigorous exertion, hyperthermia, dehydration, hypoglycemia, mental stress, and fatigue all increase sympathetic nervous system activity, which in turn shunts blood away from the GI viscera to provide increased supply to working muscles. Exercising at 70% of maximum oxygen uptake (VO 2 max) reduces blood flow to the GI tract by 60% to 70%, and higher intensity exercise may result in GI blood flow reductions exceeding 80%. Subsequent impairment in oxygen delivery to GI tract structures may result in mucosal injury, increased gut mucosal permeability, increased risk for occult blood loss, translocation of protective bacterial flora, and the generation of endotoxins. These changes contribute to typical ischemia-associated GI symptoms including nausea, vomiting, abdominal pain, and bloody diarrhea. Ter Steege et al. have postulated that the GI complaints of athletes relating to gut ischemia are the result of a reperfusion injury after exercise has ceased. Reperfusion after ischemia may result in a number of chemical and vascular changes that result in “leaky mucosa.” When this phenomenon occurs, the GI tract partially loses its barrier ability to protect itself from inherently irritating intraluminal substances such as endotoxins, food antigens, digestive enzymes, and bile.
Impact of Nutrition and Hydration
The overall fluid status of athletes has been shown to play an important role in the relative GI toxicity of high-level activity. Dehydration contributes significantly to GI tract dysfunction because it further accentuates the intrinsic blood flow changes associated with exercise. Research has shown that 80% of runners who lost at least 4% of their body weight from fluid losses during exercise experienced lower GI tract symptoms. Exercise-related fluid and electrolyte shifts result in intracellular electrolyte imbalances and cell dysfunction, which may lead to colonic smooth muscle and mucosal irritation. In runners with restricted water intake, GI symptoms are more likely to arise as a result of increases in upper GI tract and intestinal permeability relative to resting persons. In a study of nutritional intake patterns in endurance athletes, it was shown that high rates of carbohydrate intake (up to 90 g/hour) were associated with an increased risk for nausea and flatulence. In contrast, ingestion of a lower carbohydrate liquid meal before exercise is generally well tolerated, may help maintain GI tract perfusion, and may prevent gut ischemia related to decreased splanchnic blood flow.
Upper Gastrointestinal Tract Conditions
Upper GI tract complaints are common among athletes, with rates ranging from 30% to 70%. The prevailing upper GI tract conditions in athletes are gastroesophageal reflux disease (GERD) and dyspepsia. When assessing the pathophysiology behind the high rate of upper GI tract symptoms in athletes, three primary mechanisms have been postulated: (1) mechanical forces, (2) alterations in GI tract blood flow as previously noted, and (3) neuroendocrine changes that influence overall GI tract function. Mechanical forces include increased abdominal pressure from straining in high-exertion activities such as weightlifting, mechanical trauma to the GI tract from repetitive motion of the abdomen during exercise, and the impact of body position during exercise such as the flexed/compressed position of cyclists. GI mucosal activity and alterations in absorption may result from mechanical factors or neuroendocrine changes. Neural activity changes such as increased sympathetic nervous system activity, decreased parasympathetic nervous system activity, and the secretion of a number of vasoactive substances in response to exertion have all been documented to negatively influence GI tract function in athletes.
Exercise also greatly affects esophageal motility. Relaxation of the lower esophageal sphincter (LES), increased pressure gradient between the stomach and esophagus, and decreased esophageal clearance of food all have been associated with high-level physical exertion and all appear to be potentially important in the development of GERD symptoms. As exercise intensity reaches or exceeds 90% VO 2 max, the frequency and duration of esophageal reflux episodes increases. The type of exercise also influences esophageal motility; running has been found to decrease upper GI tract motility more than cycling, and studies have shown that weightlifters have the highest rate of heartburn and esophageal reflux, with correspondingly lower rates found in runners and cyclists.
Gastroesophageal Reflux Disease
GERD is the most common cause of upper GI tract symptoms in athletes. These symptoms are from the irritating effects of acidic gastric secretions as they reflux into the esophagus as a result of the loss of competence of the lower esophageal sphincter. The incidence of GERD increases with intensity of exercise, is more common in endurance sport athletes, and is exacerbated by postprandial exercise; runners demonstrate a threefold increase in GERD symptoms when running 45 minutes after completing a meal compared with running in a fasting state. Activities with large increases in intraabdominal pressure, most notably weightlifting and cycling, contribute to higher rates of symptomatic GERD in those groups as well.
Cardinal features of GERD include heartburn, retrosternal burning, and regurgitation with a sense of refluxed gastric contents into the mouth or hypopharynx. The majority of athletes with true exertional GERD actually have GERD at rest as well, and thus the greatest risk factor for GERD symptoms in the setting of exercise is the presence of GERD symptoms at rest.
Although precise GERD mechanisms are not well defined, suggested mechanisms include inappropriate relaxation of the LES ; gastric dysmotility; enhanced pressure gradient between the stomach and esophagus in sports such as football, weight-lifting, and cycling; gastric distension; delayed gastric emptying; and increased mechanical stress by bouncing of organs.
Normal peristaltic motions of the esophagus, which aid in ensuring that the acidic contents of the stomach remain in the stomach and do not migrate superiorly into the neutral environment of the esophagus, decrease in the setting of higher levels of activity. Thus any food or fluid intake that fails to pass through the stomach prior to exercise predisposes the athlete to reflux. Certain food types are well known to decrease LES pressure, such as high-fat foods (e.g., fried foods, creamy sauces, and gravy), coffee, caffeine, chocolate, peppermint, alcohol, acidic foods such as tomatoes and onions, and tobacco products. In persons who exercise, the widespread use of nonsteroidal antiinflammatory drugs (NSAIDs) also may have a negative impact on the proximal GI tract because of their inherent propensity to irritate the GI tract as a result of the suppression of protective prostaglandins.
GERD, Asthma, and Other Related Conditions
GERD may present with a number of less typical symptoms including cough, sore throat, hoarseness, asthma, bronchitis, recurrent pneumonia, intermittent choking, or chest pain. Athletes presenting with any of these symptoms or complaints should be considered as potentially having GERD. Many of these persons have “silent” reflux that fails to generate the classic GI manifestations. GERD can provoke or exacerbate asthma by either silent aspiration into the tracheobronchial tree or by stimulating an acid-mediated esophagobronchial reflex that provokes dyspnea and wheezing. It is estimated that up to 90% of persons with asthma have GERD and up to 40% of persons with asthma have esophagitis. However, research to date has only shown benefit for asthmatic symptoms in patients with nocturnal GERD symptoms. Persons with only daytime GERD symptoms did not demonstrate improvements in their asthma status as a result of aggressive GERD treatment. It is always important to consider GERD as the potential primary pathology in an athlete who has new or unusual asthmatic symptoms.
Several clinical variants of GERD are also recognized. Laryngopharyngeal reflux disease is typically manifest by hoarseness, voice change, and chronic cough. It is believed to result from an esophageal reflux mechanism with secondary inflammation and damage of the proximal airway and laryngeal area. Duodenogastroesophageal reflux results from reflux of duodenal, rather than gastric, contents, including biliary secretions, pancreatic enzymes, and bicarbonate. Duodenogastroesophageal reflux is believed to represent one of the causative factors for refractory GERD despite appropriate management with the maximal dose of medications. Finally, a number of proposed extraesophageal manifestations of GERD include recurrent pharyngitis, otitis media, sinusitis, and pulmonary fibrosis.
The importance of proper GERD management cannot be overstated, not only to prevent acute symptoms and their impact on performance in sports but also to decrease the risk of long-term complications, including peptic strictures and Barrett esophagus with its potential for malignant transformation. Successful GERD management includes lifestyle modifications, use of medications, or both. Lifestyle modifications should always be the first-line treatment in athletes who have GERD. These modifications include sleeping on two pillows to enhance gravity-associated esophageal clearance, avoidance of lying down to sleep within 4 hours of the evening meal, avoiding postprandial exercise, and limiting consumption of foods known to relax the LES, as previously noted. Athletes should also avoid consuming solid food and high-carbohydrate drinks prior to strenuous activity. Rather, they should consume liquid meals with lower carbohydrate content and ensure adequate hydration. Sports drinks containing up to a maximum of 10% glucose are believed to be the optimal calorie-containing beverages for training with a low tendency to cause upper GI tract symptoms.
If these interventions fail to improve symptoms, pharmacologic therapy should be considered. The two primary medications used to treat GERD include H2-receptor antagonists (e.g., ranitidine and famotidine) and proton pump inhibitors (PPIs; e.g., omeprazole and pantoprazole). Initially, a 2-week trial of PPI therapy given daily 30 minutes before the morning meal is a generally accepted first-line treatment. If once-daily therapy is insufficient, PPI dosing should be doubled. If it is initially effective, completion of an 8-week course is generally appropriate and effective for long-term benefit, particularly if combined with lifestyle measures. If symptoms recur within 3 months, additional evaluation to solidify the diagnosis is generally warranted, and if symptoms are truly GERD-related, they may be best managed with ongoing PPI therapy.
If GERD symptoms are limited to discreet competitive times, it has been shown that markers of exercise-induced gastroesophageal reflux—percentage reflux time and number of reflux episodes—can also be effectively reduced by pretreatment with an H2-receptor antagonist (e.g., 300 mg ranitidine) 1 hour prior to activity.
Upper endoscopy is the evaluation tool of choice for diagnosis confirmation and is also indicated for clinical presentations with a greater cause for concern, including failure of empiric therapy as previously described, the need for continuous therapy, the presence of atypical symptoms such as odynophagia, dysphagia, weight loss, bleeding, or anemia, or long-standing symptoms. Additional workup should include Helicobacter pylori testing to exclude its potential role in non-GERD syndromes such as peptic ulcer disease and nonulcer dyspepsia. Confirmation of H. pylori infection is most effectively achieved via a gastric mucosal biopsy at the time of upper endoscopy or via serologic testing or a urea breath test. If such testing is positive, a triple-drug 2-week antibiotic/acid suppressive treatment course should be pursued.
Studies reveal that up to 60% of persons presenting with signs and symptoms compatible with GERD but who fail to respond to aggressive PPI therapy have a syndrome referred to as “functional heartburn.” The Rome III diagnostic criteria for functional heartburn include burning retrosternal discomfort or pain, absence of evidence that GERD is the cause of the symptom, absence of an esophageal motility disorder, and symptom onset of at least 6 months. As such, this diagnosis can only be made after a formal referral to a gastroenterologist and the completion of an appropriate diagnostic workup.
Functional heartburn is also known as “esophageal hypersensitivity” and bears resemblance to other common GI disorders that include a pattern of visceral hyperalgesia, such as irritable bowel syndrome (IBS). Management is challenging, and many persons continue to have symptoms despite undergoing therapy. Biofeedback in an effort to modify nervous system input to the GI tract is the treatment of choice. Tricyclic antidepressants and prokinetic agents also have potential value, but their significant adverse effect profiles are generally incompatible with participation in sports.
Dyspepsia refers to a spectrum of vague GI symptoms including gnawing or burning epigastric pain, nausea, vomiting, eructation, bloating, indigestion, generalized abdominal discomfort, and early satiety. The three most common causes of dyspepsia in athletes include GERD, gastritis, and peptic ulcer disease. In addition, many drugs are associated with dyspepsia, including NSAIDs, antibiotics, and estrogens. In fact, most drugs have a potential to cause dyspepsia in at least some patients.
Regardless of the cause of dyspepsia, the common pathologic feature is mucosal damage of the upper GI tract. Gut mucosal injury in athletes may be multifactorial from mucosal ischemia, dehydration, stress of competition, and excessive use of NSAIDs, medications, alcohol, caffeine products, or dietary supplements. These same factors increase the risk for upper GI tract bleeding and ulcer disease in athletes. Upper GI evaluations in professional long-distance runners revealed at least one GI mucosal lesion in approximately 90% of the runners even in the absence of symptoms. Further supporting the role that dyspepsia plays in damaging the upper GI tract, data show that use of a PPI in ultramarathon runners has significantly decreased their incidence of GI tract bleeding.
Dyspepsia management focuses on the limitation or elimination of the aforementioned provocative factors. Should those interventions provide inadequate benefit, acid suppressive therapy with H2 blockers or PPIs is the pharmacologic treatment of choice. For persons with chronic dyspepsia or who have had frank GI bleeding with heavy exercise, consistent use of a PPI or H2 blocker is reasonable and likely prudent in preventing symptoms or complications from upper GI tract damage.
Impact of Aspirin and NSAIDs
Aspirin and NSAID use places the GI tract at risk because of the blockade of cyclooxygenase and the subsequent loss of constitutive cytoprotective gastric prostaglandins. Although NSAIDs clearly are linked to a risk of gastritis and peptic ulcer disease with prolonged use, they have yet to be shown to correlate with risk for GI bleeding in endurance athletes. Whenever feasible, it is advisable to have athletes minimize the use of NSAIDs; however, the need for pain and inflammation management in highly active persons makes complete avoidance of NSAIDs largely unrealistic. For athletes who require NSAIDs to maximize performance, particularly if they have a previous history of ulceration or bleeding, it is prudent to add a daily PPI for GI tract protection.
Pill esophagitis results from the local irritating effects of certain medications if they remain in the esophagus for a prolonged period. In athletes, NSAIDs are the classic family of medications with greatest risk. The tetracycline antibiotic family, which often is used in athletes on a chronic basis for acne or in shorter-term courses for tick-borne illness, and the antimalarial drug mefloquine are notoriously problematic for this condition as well. Prevention is best achieved by taking medication in the morning with food or a moderate volume of liquid, remaining upright after pill ingestion, and avoiding bedtime dosing. It is always prudent to educate athletes about a medication’s risk for GI toxicity as well.
Dysphagia is a condition characterized by difficulties with swallowing that are typically driven either by alterations in nerve or muscle function. Sport-associated dysphagia is most commonly caused by the irritative effects of GERD, although any intrinsic esophageal disorder may be responsible. Underlying neurologic diseases most commonly associated with dysphagia such as multiple sclerosis and Parkinson disease are significant and generally incompatible with anything above recreational exercise.
Clinically, dysphagia is divided into two subtypes based on anatomic location and pathologic mechanism. Oropharyngeal dysphagia typically presents with greater difficulty in swallowing liquids than solids and is characterized by repeated attempts to swallow due to a sensation of choking or incomplete swallowing. Oropharyngeal dysphagia occurs within the first second of the initiation of swallowing and presents with odynophagia that localizes to the neck. Other characteristics may include a change in dietary habits, dehydration, regurgitation, or unexplained weight loss. In contrast, esophageal dysphagia presents with difficulty swallowing both solids and liquids, occurs several seconds after the initiation of swallowing, and is characterized by odynophagia that localizes to the substernal area. Dysphagia management focuses on addressing presumptive GERD or identifying and subsequently managing other underlying conditions.
Nausea and Vomiting
Nausea and vomiting may be experienced by athletes in association with strenuous or prolonged exercise. Although the etiology is not always clear and may create a challenge for prevention and management, postprandial exercise is most clearly linked to the incidence of nausea and vomiting. Reflux of stomach contents coupled with changes in esophageal motility, sphincter tone, and GI ischemia likely contribute to the increased incidence of nausea and vomiting associated with exercise. However, nausea and vomiting do not have to be associated with heavy exertion. Athletes may have these manifestations even when they are relatively inactive, a phenomenon supported by research in runners who demonstrated a higher incidence of bloating and vomiting when they were not training.
Prevention of nausea and vomiting focuses on prudent dietary and fluid choices to minimize gastric irritation or altered GI absorption. In keeping with general intake guidelines, for events lasting less than 1 hour, optimal energy supplementation to minimize GI effects is provided by sports drinks with carbohydrate concentrations of 6% to 8%. For longer duration activities, carbohydrate intake of 30 to 60 g/hour should be well tolerated and effective. Athletes should also avoid eating solid food within 3 hours of an athletic event. Finally, because NSAID use has been shown to increase nausea and vomiting in endurance runners, caution should be exercised in their use around the time of athletic participation even for activities of shorter duration. If nausea is associated with prominent heartburn during activity, a trial of an H2 blocker or PPI may be warranted. Studies have shown that both H2 blockers and PPIs can be helpful for exercise-related nausea, and the sports medicine provider should have a low threshold for the treatment of affected athletes when they are participating in activities that are likely to provoke symptoms.