Evaluation of athletes with exertional abdominal pain has not been commonly written about in the medical literature, despite 33% of runners reporting abdominal pain (5), and up to 50% of athletes having gastrointestinal symptoms during heavy exercise. Other statistics include 30%-60% of long distance runners experiencing symptoms (26) and 25%-50% of elite athletes being sidelined by gastrointestinal symptoms (18). In discussion with colleagues about this topic, one suggestion offered is that, by definition, exertional pain should resolve after activity, leading us to believe that it is of a benign etiology. However, when this pain is recurrent and interferes with an athlete‘s training or competition, an evaluation is likely in order to distinguish functional (and presumably benign) pain from an underlying disorder. The goal of this article is to review relevant changes of the digestive tract during exercise, provide a differential diagnosis of causes of exertional abdominal pain, and conclude with a proposed mechanism for evaluation of exertional abdominal pain. A Medline literature search was conducted with a focus on articles from the past 5 yr (2004-2009).
THE GASTROINTESTINAL TRACT
While we know the general health benefits of mild-to-moderate exercise (reduction in rates of cardiovascular disease, hypertension, hyperlipidemia, insulin resistance, colon cancer), we also must acknowledge that intense exercise may result in complaints of gastrointestinal dysfunction and abdominal pain. The most common reported exertional upper gastrointestinal symptoms include heartburn, chest pain, epigastric pain, bloating, belching, regurgitation, nausea, vomiting, and abdominal cramps (18,20). In a study of 606 athletes, 36% of runners, 67% of cyclists, and 52%-54% of triathletes reported some of these symptoms (12). The prevalence of pain and gastrointestinal complaints increased with younger athletes and with longer bouts of exercise (5,12,16). Lower gastrointestinal complaints, such as the urge to defecate, diarrhea, and constipation, also are commonly reported by athletes (26). Alterations in the physiology of the digestive system in exercise may contribute to these complaints, and the frequency with which these symptoms occur makes it important for us to understand these changes.
With the onset of activity, changes in hormone levels result from the stimulation of sympathoadrenal activity and pituitary secretion. This increase in sympathoadrenal activity is important for appropriate cardiac output and heat regulation, where blood flow is diverted to muscles and skin (18). Stimulation of the hypothalamus-pituitary-adrenal axis also leads to decreased levels of insulin and increased digestive peptides and immunosuppressive hormones, such as cortisol. This increase in catecholamines suppresses the thirst drive, which can lead to dehydration and further exacerbate gastrointestinal complaints (18), and decreases gastrointestinal motility (12,20). Exercise also has been shown to affect motilin and gastrin, which increase gastrointestinal motility (12,20).
Controversy exists as to the alteration of gastrointestinal motility with exercise. Evidence regarding esophageal contractions includes decreased duration and amplitude (9,26), and decreased (9,26) and increased frequency of contractions (9). Reports on gastric emptying range from decreased gastric motility with activity (26) to changes dependent on intensity of exercise: decreases at 70%-90% of V˙O2max (12,18), but less intense exercise may have no effect (12) or increase emptying (12,20). There also is conflicting evidence regarding effect on small bowel and colonic motility (18). One comprehensive study tested 10 healthy males with no previous history of exercise-associated gastrointestinal disturbances and measured esophageal motility, gastroesophageal reflux, gastric pH, oral-cecal transit time, gastric emptying, and intestinal permeability and glucose absorption. Each subject acted as his own control in an exercise and rest protocol. Significant differences during cycling, compared with rest, were found in the following: increased esophageal peristaltic velocity, decreased contraction pressure at the mid esophagus, decreased peristalsis at the mid and distal esophagus, and decreased absorption of glucose (28). Although this study was published 10 yr ago, it is significant because it measured all of these parameters simultaneously, which to this author's knowledge had not been accomplished previously or since.
As blood is preferentially shunted to muscle, heart, lung, and brain during exercise, splanchnic perfusion is decreased. Blood flow can be reduced by as much as 80% (12,18,26). At maximal exercise, splanchnic flow decreases from 1.56 L·min−1 to 0.3 L·min−1 (26). As with any other tissue in the body, this decrease in perfusion depletes adenosine triphosphate (ATP), and cell death and inflammation ensue. Dehydration can further exacerbate this ischemia (18), causing pain and/or diarrhea. Exercise also enhances mucosa permeability, which increases translocation of bacteria and endotoxins, which may contribute to nausea, vomiting, and diarrhea (18,26).
Finally, physical exertion is transmitted to intraabdominal organs via two mechanisms: increased intraabdominal pressure and increased movement of the organs themselves. Elevated intraabdominal pressure can overwhelm the lower esophageal sphincter, transient lower esophageal sphincter (LES) relaxation can occur (12,20) and exacerbate or induce reflux (18). The increased mobility of organs can cause gastrointestinal symptoms and pain as well (18).
OBTAINING A HISTORY OF EXERTIONAL ABDOMINAL PAIN
As with any complaint that a patient presents with, a thorough history and physical are essential in guiding your differential diagnosis. In addition to a routine abdominal pain history (location, onset, palliation/provocation, quality, radiation, severity, timing, relation to meals and bowel movements, associated symptoms such as nausea, vomiting, diarrhea, constipation, urge to defecate), there are specific questions to focus on with athletes. A detailed exercise and training history is important to establish, for example, any recent increases or changes in amount, type or intensity of exercise, any new exercises, and how long have they been at their current fitness level. A complete diet history also is important, including supplements, fluid, and meal composition (what is eaten, how frequently they are eating, timing of meals in reference to activity, and when pain strikes), hydration status, and what they are hydrating with (water vs electrolyte replacement). These factors may be contributing to their symptoms. Modifications in diet (e.g., not eating large meals before exercise), hydration techniques, and gradual increases or alterations in activity can be diagnostic and therapeutic if pain and symptoms improve with institution.
DIFFERENTIAL DIAGNOSIS OF EXERTIONAL ABDOMINAL PAIN: COMMON REPORTS IN THE LITERATURE
Based on the history given by the athlete, we should form a differential diagnosis and then use physical exam and testing to confirm. This section will focus on common etiologies of exertional pain reported in the literature. The Table summarizes the differential diagnosis and evaluation of exertional abdominal pain.
Exercise-related transient abdominal pain (ETAP), more commonly referred to as stitch, classically has been described as localized and transient, and 90% of those experiencing it report one of the following characteristics: sharp, stabbing, cramping, aching, or pulling. A survey conducted at a community run in Australia reported a prevalence of ETAP in 27% of the 848 participants (16). In a previous study, Morton and Callister reported a 60% prevalence of ETAP in runners over the previous year (15). Numerous causes have been hypothesized and reported, including diaphragmatic ischemia, subdiaphragmatic ligament stress, and irritation of parietal peritoneum (7,14-16). Skeletal muscle cramp previously was thought to explain ETAP; however, it has since been demonstrated that there is no increase in electromyography (EMG) activity at the site of ETAP (15). A classic history provided by the athlete (as described previously in this article) and a normal physical exam may be adequate in establishing the diagnosis of ETAP (7).
Gastroesophageal reflux disease (GERD) occurs in approximately 10%-20% of people in Western countries and in 50%-60% of athletes (18,20). In athletes, GERD is more common during exercise than at rest (18,20,26), and intense, but not moderate, exercise has been shown to increase symptoms (9,12). Both the number and duration of episodes increase with intensity at 90% V˙O2max (18,20,26). Weightlifters seem to be more susceptible to reflux (18,26), likely because of increases in intraabdominal pressure (12). Runners and cyclists report less frequent episodes, with runners having more than cyclists (18,26), likely from jostling of abdominal organs. Definitive diagnosis of GERD can be made by 24-h pH monitoring and/or endoscopy (12,20). Alternatively, clinicians may offer a trial of lifestyle modifications or a trial of H2 blockers or proton pump inhibitors (12) before invasive testing based on history and exam, where resolution of pain and symptoms would establish the diagnosis.
Gastrointestinal ischemia is a less common, but serious etiology of exertional abdominal pain. Typical symptoms include pain (during meals and/or activity) and diarrhea, which are thought to be protective in limiting further damage (17). Diagnosis of intestinal ischemia traditionally has included a strong clinical suspicion and angiography of the splanchnic vessels. In a study of additional screening and diagnostic methods, Otte et al. found that screening suspected cases with less invasive methods - gastric tonometry (to demonstrate ischemia) and duplex sonography of the celiac artery and superior mesenteric artery (to demonstrate stenosis), and then angiography if either were abnormal or inconclusive - is an alternative method. This resulted in 100% negative predictive value (not missing any cases of ischemia), while avoiding 21% of angiographies (19). Noninvasive diagnostic methods include computed tomography angiography (CTA) and magnetic resonance angiography (MRA). According to Shih and Hagspiel, CTA probably is the most frequently used technique, as calcified plaques, the inferior mesenteric artery, and peripheral splanchnic branches are better visualized. MRA is useful when exposure to radiation must be avoided (25).
Musculoskeletal problems also can account for exertional pain. Abdominal wall pain should be suspected when pain is related to specific movements or can be localized with one or two fingers. The most frequent sites of abdominal wall pain are the linea semilunaris, linea alba, rectus muscle, and along the cartilagenous portion of the ribs, in descending order. Cutaneous nerve entrapment, myofascial trigger points, forceful contractions causing skeletal muscle strain, bloating straining the abdominal wall, and radiculopathy have been proposed as mechanisms of pain (10). Rare reports of abdominal wall rhabdomyolysis exist, including an amateur boxer who recently increased his training to include over 500 abdominal crunches and had been binge drinking over the previous few days (3). Traditionally, these reports of rhabdomyolysis have occurred in military recruits but should be suspected in an athlete with a similar history of rapid increase in repetitive training movements, and can be confirmed with elevated creatine kinase levels. Rib stress fractures also may be seen in sports requiring repetitive strain, such as rowing, swimming, throwing, and golf. Stress fracture pain typically has an insidious onset and worsens until the activity can no longer be performed because of pain. Pain usually can be localized with one finger by the patient, and stress fracture can be confirmed with plain x-ray, bone scan (13), ultrasound, computed tomography (CT), or magnetic resonance imaging (MRI). In a study of 50 subjects who presented to the emergency room after chest wall trauma, x-ray identified 8 fractures in 6 patients, whereas sonography (within 3 d) identified 83 fractures in 39 of the same patients. A follow-up ultrasound 3 wk later was able to demonstrate healing of identified fractures and diagnosed 12 additional fractures in 9 patients. Ultrasound, while more time-consuming than x-ray, can offer increased sensitivity at diagnosing rib fractures without exposure to radiation (11). Finally, a sports hernia may account for exertional lower abdominal or, more commonly, groin pain. This type of hernia is the result of a weakness or tear of the posterior inguinal wall and usually is not apparent on physical exam. In addition, imaging studies (x-ray, bone scan, and MRI) tend to be normal or show nonspecific findings, and they usually are obtained to rule out other pathology. Ultrasound may be useful in demonstrating abnormality, but asymptomatic individuals may have the same findings. Sports hernia is most common in male athletes who participate in sports with repetitive twisting and turning, and the pain does not usually improve without surgical treatment (8).
Exertional abdominal pain also can be referred pain from cardiorespiratory dysfunction. Cardiac causes may include myocardial infarction (MI). History of hyperlipidemia, personal or family history of cardiovascular disease, or atherosclerotic disease may increase one's index of suspicion. MI can be ruled out with a normal electrocardiogram (EKG) and serial troponins. Cardiac function can be assessed with echocardiogram, and stress testing can include EKG or echo. Asthma also may present as exertional abdominal pain, especially in younger athletes. A diagnosis can be made with pulmonary function testing (23), and provocative testing includes exercise testing, eucapnic voluntary hyperventilation (EVH), and methacholine challenge (24). EVH has been the standard for documenting exercise-induced bronchospasm by the International Olympic Committee and is performed by having a subject inhale a CO2 gas mixture at a predetermined rate for 6 min. This predetermined rate may be defined as 30 times their forced expiratory volume in 1 s (FEV1) (2,24). These conditions are proposed to simulate exercise conditions. In a study of 38 Olympic-level athletes, EVH was compared with field exercise testing, where a drop in FEV1 of greater than or equal to 10% of baseline was defined as a positive test. Subjects were tested with both methods on different days, and EVH identified eight extra subjects missed by exercise testing, while only missing two subjects who were diagnosed with exercise testing (24). While EVH typically has been used in elite athletes and research settings, Brummell et al. has demonstrated usefulness in a pulmonary clinical practice, where testing was diagnostic and well tolerated (2).
Alternative diagnoses may include, although less likely and not specifically documented in the literature, exertional heat illness that can be ruled out with a normal core temperature, psychiatric illness such as anxiety or depression, infection that may be suspected with a history of diarrhea and recent travel and confirmed with stool studies, and inflammatory bowel disease evaluated with endoscopy. In hypothyroid athletes, common gastrointestinal symptoms such as constipation may incite or exacerbate pain.
DIFFERENTIAL DIAGNOSIS OF EXERTIONAL ABDOMINAL PAIN: CASE REPORTS IN THE LITERATURE
Types of articles on the more common causes of exertional abdominal pain may be written as review articles or original studies; however, rare etiologies of exertional abdominal pain typically are documented as case reports. Hypoferritinemia was reported as the cause of exertional abdominal pain in a cross-country runner who had a 6-month history of pain. Initially, she was thought to have reflux, but her symptoms did not improve with empiric treatment. Further investigation revealed iron deficiency without anemia and hypoferritinemia, and after 6 wk of supplementation, she had complete resolution of symptoms (4).
A case report of a long-distance runner with a 12-yr history of right upper quadrant pain with strenuous exercise revealed the cause to be congenital supernumerary ligaments binding the gallbladder to the abdominal wall. The diagnosis was made only after a laparoscopy, and after cholecystectomy, the patient's pain resolved (5).
There also are rare reports of exercise-induced cholangitis and pancreatitis in patients with prior surgery releasing the sphincter of oddi, which regulates pressures transmitted from the duodenum. When the sphincter is no longer functioning, duodenal contents are able to reflux into the pancreatobiliary tract. This may be suspected in a patient with a surgical history of biliary bypass or pancreatoduodenectomy, with symptoms of fevers, right upper quadrant (RUQ) abdominal pain and jaundice (cholangitis) or epigastric pain, nausea and/or vomiting, and elevated pancreatic enzymes (27).
Postexertional abdominal pain also has been documented in the literature. Cecal-slap syndrome was reported in the 1980s, where repetitive slapping of the cecum in a marathoner was believed to account for postexertional abdominal pain and diarrhea (21). The following cases described are reported associations and are not meant to imply any cause and effect. Pruett et al. describes two runners who reported sudden onset of abdominal pain. They ran 50-60 miles·wk−1 and neither had ever had abdominal surgery. On barium enema, they were found to have a cecal volvulus and required resection (22). Of interest, this author is a third case of cecal volvulus with a similar history: a runner, never had abdominal surgery, sudden onset of epigastric pain, diagnosed with cecal volvulus at the age of 28, and required a right hemicolectomy. Recent reports include postexertional appendicitis in a marine after running a marathon (6) and acute pancreatitis diagnosed on CT scan in a football player, with subsequent endoscopic retrograde cholangiopancreatography (ERCP) demonstrating the anomalous cause of pancreatitis: the patient's common bile duct emptied into his pancreatic duct (1).
EVALUATION OF EXERTIONAL ABDOMINAL PAIN
As discussed previously in this article, a complete physical exam ultimately should confirm the diagnosis established with the patient's history. The following routine tests may be recommended: EKG with consideration of a stress EKG, complete blood count (CBC), erythrocyte sedimentation rate (ESR), electrolytes, hepatic and pancreatic function markers, fecal occult blood (FOB), and a fasting lipid profile. This initial workup can help rule in or out some of the common gastrointestinal diagnoses found among athletes: ETAP, GERD, diarrhea, gastrointestinal bleeds (18), esophagitis, gastritis, ulcers, and diseases of the gallbladder and biliary system (5).
Additional labs to consider after the initial workup include: markers of muscle injury such as lactate dehydrogenase (LDH) and creatine kinase, iron studies and ferritin levels, thyroid-stimulating hormone (TSH), and stool studies. GERD typically is a clinical diagnosis based on history and a trial of treatment via lifestyle modifications or empiric medications; however, 24-h pH probe monitoring (even exertional monitoring) and endoscopy also can be used. Diagnostic tests include echocardiogram and abdominal ultrasound.
Less common etiologies may be evaluated with x-ray, bone scan, ultrasound, CT or MRI for stress fracture, and EVH, exercise testing, and pulmonary function testing (PFT) for asthma. Evaluation of suspected gastrointestinal ischemia may include CTA, MRA, gastric tonometry, duplex sonography of the celiac artery and superior mesenteric artery, and angiography as needed. In rare cases, as reported previously in this article, when all other causes of abdominal pain have been excluded, a laporoscopy may be considered.
As discussed previously in this article, a complete history, including focus on diet, hydration, supplementation, and physical activity, and a complete physical exam are important in guiding the differential diagnosis and subsequent evaluation of exertional abdominal pain. While certain issues are common (GERD, ETAP, GI complaints), additional laboratory testing can establish or rule out underlying pathology. Dimeo, Peters, and Guderian (5) summarize when a further evaluation is likely necessary: ``New complaints during exertion in an experienced and previously asymptomatic athlete, the absence of triggering factors such as trauma or dietary excess, a change in the pattern, duration, or severity of pain, or the persistence of symptoms after exertion all suggest an underlying disorder.'' While the athletes we work with tend to be healthy, it is important not to overlook more serious medical conditions that they, too, may have.
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