Clin Sports Med 24 (2005) 525–540
CLINICS IN SPORTS MEDICINE
Training Room Management of Medical
Conditions: Sports Gastroenterology
Ellen Casey, MDa, Dilaawar J. Mistry, MD, ATCb,*,
John M. MacKnight, MDc
a
University of Virginia School of Medicine, Charlottesville, VA, USA
Department of Physical Medicine and Rehabilitation, University of Virginia Health System,
545 Ray C. Hunt Drive, Suite 240, Box 801004, Charlottesville, VA 22903, USA
c
University Physicians Internal Medicine, University of Virginia Health System, 415 Ray C. Hunt Drive,
Suite 2100, Charlottesville, VA 22908, USA
b
G
astrointestinal (GI) illnesses are common in athletes. Various causes
include adverse physiologic adaptations of the gut during exercise;
excess ingestion of carbohydrate drinks, alcohol, and anti-inflammatory medications; emotional stressors; exposure to pathogens in closed environments and during travel; trauma; and abdominal wall pressure overload.
Commonly encountered conditions in this population include self-limited food
poisoning, gastroesophageal reflux disease (GERD), hiatal hernia, irritable
bowel syndrome (IBS), and viral gastroenteritis. More serious conditions such
as Crohn’s disease (CD), ulcerative colitis (UC), appendicitis, mesenteric adenitis, and invasive diarrhea are far less common in this population and generally
present dramatically with abdominal pain, nausea, vomiting, and bloody diarrhea. Vigilance for such conditions is essential; however, timely diagnosis and
treatment can be delayed as most athletes have enhanced pain tolerance, often
do not verbalize their symptoms in a timely manner, and frequently indulge in
self-medication prophylactically and therapeutically.
Unfortunately, evidence-based management of GI illnesses in athletes is limited because most studies have compared various GI illnesses between different
sports, rather than comparing athletes to nonathletes. This article reviews the
evidence that is available specifically relating to etiology, pathophysiology, clinical presentation, relevant differential diagnoses, acute management, and recommendations for specialist consultation of various GI illnesses in the training
room setting.
* Corresponding author. E-mail address: [email protected] (D.J. Mistry).
0278-5919/05/$ – see front matter
doi:10.1016/j.csm.2005.05.002
© 2005 Elsevier Inc. All rights reserved.
sportsmed.theclinics.com
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PHYSIOLOGIC ADAPTATIONS OF THE GASTROINTESTINAL
TRACT: EXERCISE CONSIDERATIONS
Regular, moderate physical activity promotes several health benefits for the GI
tract. Physiologic digestive processes, such as gut emptying, are enhanced [1]
and there is a reduced incidence of liver disease [2], cholelithiasis [3], colon
cancer [2], and constipation [4,5]. Conversely, frequent, high-intensity exercise
causes undesirable symptoms such as heartburn, chest pain, bloating, belching,
nausea, vomiting, abdominal cramps, frequent urge to defecate, diarrhea, and
constipation. These symptoms are reported by approximately 20% to 50% of
high-performance athletes, are more commonly encountered in women than
men, are more common in younger athletes, and are less frequent in sports that
incorporate more gliding movements, such as cycling [1,5–8]. However, there is
a lack of difference between the number of reflux episodes, gastric emptying
(GE), transit time, and intestinal permeability and glucose absorption between
runners and cyclists at rest [8]. Therefore, exercise-induced GI distress is not a
result of a particular GI phenotype that makes certain individuals more susceptible to the plethora of undesirable symptoms. Although the precise mechanisms
for the various GI symptoms are poorly understood and studied [9], several
theories and a few studies have postulated the potential detrimental alterations
in GI function commonly encountered in competitive athletes.
For example, gut ischemia secondary to attenuated GI blood flow [8,10] is a
well-defined exercise adaptation that redirects blood flow to active muscles and
the pulmonary vasculature [11]. Exercise typically reduces GI blood flow in
excess of 50% [12], which makes the gut mucosa susceptible to ischemic injury
[13]. Mucosal injury increases gut mucosal permeability, enhances occult blood
loss, and induces translocation of protective bacterial flora and generation of
endotoxins that can induce diarrhea [8,14]. Other suggested mechanisms for
increased GI distress include increased vibration of the abdominal wall and
bouncing of the organs, especially in runners [6,8] and various neuroimmunoendocrine adaptations to exercise. Increased catecholamines and 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 [5,8,11,15].
Additionally, wide-ranging fluid intake and dietary patterns through largely
hormonal mechanisms can further alter homeostasis of the GI tract. For example, GE is slowed by high-intensity exercise [2,16,17] following consumption of
beverages in a dehydrated state [18], and is independent of either training status
[19] or gut blood flow and plasma volume [20]. The excitement of competition
elevates circulating catecholamines that are known to suppress thirst [21,22].
Furthermore, athletes are frequently averse to the unpleasant sensation of a full
stomach during competition. Therefore, it is not uncommon to delay hydration
during competition, which in turn may expedite fluid and electrolyte imbalance.
GI distress secondary to slowed GE [20] has been reported by up to 40% of
dehydrated athletes who consumed a 7% carbohydrate beverage, as compared
to euhydrated counterparts [18]. GE can be further slowed by the consump-
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tion of more palatable hypertonic carbohydrate beverages after 20 minutes
of running [23]. Conversely, excessive fluid intake that produces shifts in osmotic pressure [11], and excessive consumption of food rich in fat, protein, and
fiber in proximity to the onset of competition can also promote undesirable GI
symptoms [24]—an effect that is magnified by increased postprandial motor
activity [25] and enhanced gut transit time observed following physical activity
[8,26].
In summary, various physiologic adaptations to exercise make competitive
athletes more susceptible to GI distress.
DYSPHAGIA
The swallowing mechanism is a complex process involving several closely
coordinated voluntary and reflexive actions within the oropharynx and esophagus. Dysphagia, a common swallowing disorder in the athletic population, is
most commonly caused by acid reflux. However, it is important to recognize
and expeditiously treat other potentially serious yet rarer causes of dysphagia.
A careful history is crucial to diagnosis and can determine the cause of
dysphagia in 80% of cases [27]. Although athletes may present with a spectrum
of complaints, a few pivotal elements of a detailed history allow anatomic
classification of dysphagia into two subclasses: oropharyngeal or esophageal.
First, does the dysphagia occur with liquids, solids, or both? Second, does the
difficulty swallowing occur soon after the initiation of deglutition or is it delayed? Finally, is dysphagia painful or painless, and if painful, does the pain
during deglutition localize to the neck or the chest?
Oropharyngeal dysphagia (OD) typically presents with greater difficulty
swallowing liquids compared with solids; is characterized by repeated attempts
to swallow secondary to a choking sensation or a sensation of incomplete
swallowing; occurs within the first second of deglutition; and presents with
odynophagia that localizes to the neck. Other characteristics may include
either a change in dietary habits, dehydration, regurgitation, or unexplained
weight loss.
Commonly encountered causes for painful OD include tonsillitis, pharyngitis, laryngitis, cervical adenitis, and thyromegaly. Other less common causes of
OD include Ludwig’s angina, retropharyngeal abscess, or anaphylaxis resulting from insect sting, drug and food allergies, or exercise.
Unlike painful OD that is induced by inflammation or mechanical pressure,
painless OD is caused by disordered neuromuscular functioning of the pharynx and upper esophageal sphincter. Causes in athletes are rare and include
Guillain-Barre syndrome (which should be suspected in an athlete presenting
with painless OD and respiratory distress following influenza vaccination),
globus hystericus as a manifestation of GERD, and laryngeal cancer in athletes
who have a history of chewing tobacco abuse.
In contrast to OD, esophageal dysphagia (ED) presents with difficulty
swallowing solids and liquids, occurs several seconds after swallowing, and is
characterized by odynophagia that localizes to the sixth thoracic dermatome
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[28]. Frequent complaints include an ill-defined substernal pressure and burning, and in severe cases, frank chest pain.
ED occurs with various mechanical and inflammatory disorders affecting
the esophageal body or its peristaltic function. Common causes of painful ED in
athletes include esophagitis induced by acid reflux [8,29] or, less commonly, infections such as herpes simplex virus, cytomegalovirus, and candida in immunocompromised individuals. Other causes include caustic injury to the lower
esophagus from bilious vomiting, or pill esophagitis following treatment with
tetracyclines, nonsteroidal anti-inflammatory drugs (NSAIDs), or alendronate.
Acid reflux may also induce diffuse esophageal spasm (DES) that presents with
symptoms similar to GERD and pill esophagitis, including noncardiac chest
pain, globus, and regurgitation. Other less common, yet important, causes of
esophageal dysphagia in the athletic population include aortic aneurysm in
athletes who have Marfanoid features; mechanical obstruction of the esophagus
from strictures, webs, or malignancy; or motility disorders, such as achalasia
or scleroderma.
Persistent dysphagia necessitates further workup and specialist evaluation.
Persistent noncardiac chest pain warrants a definitive diagnosis. Concomitant
anemia, unexplained weight loss, anorexia, and nontender cervical or supraclavicular lymphadenopathy [28] could suggest occult GI malignancy [30].
GASTROESOPHAGEAL REFLUX DISEASE
Symptomatic reflux of gastric contents into the esophagus is encountered in
approximately 60% of athletes and occurs more frequently during exercise than
at rest [31,32]. Exercise not only exacerbates GERD, as demonstrated in studies
that used ambulatory pH monitoring [33–35], but is also a contributing factor to
reflux in healthy volunteers [32]. And although proton pump inhibitor therapy
reduced acid reflux in runners, symptoms of heartburn, chest pain, and regurgitation were omnipresent, suggesting a multifactorial cause of GERD during
exercise [36].
Although the precise mechanisms are not well defined, either the isolated
effects or combination of several physiologic alterations contribute to acid
reflux during exercise. Suggested mechanisms include gastric dysmotility [29];
relaxation of the lower esophageal sphincter (LES) [8]; enhanced pressure gradient between the stomach and esophagus [32]; gastric distension [24]; delayed
gastric emptying [8,20] (especially in a dehydrated state [18]); enhanced intraabdominal pressure in sports such as football, weight lifting, and cycling [32];
and increased mechanical stress by bouncing of organs [8].
The duration, amplitude, and frequency of esophageal contractions decline
with exercise intensity at or above 90% of VO2max, and the number of
gastroesophageal reflux episodes and the duration of esophageal acid exposure
are correspondingly increased during exercise at 90% VO2max. Additionally,
increase in reflux episodes has been observed despite a lack of differences in
esophageal peristaltic velocity and pressure in symptomatic and asymptomatic
cyclists at 70% of VO2max. These data suggest that an increased number of LES
SPORTS GASTROENTEROLOGY
529
relaxations may contribute to increased reflux during exercise [8]. Thus, exercise has profound effects on acid reflux that are intensity-dependent [29].
The degree of acid reflux is also sports-specific. Collings and colleagues [32]
demonstrated that athletes involved in predominantly anaerobic sports, such as
weight lifters, experience the most heartburn and reflux. In the same study,
runners had mild symptoms and moderate reflux and cyclists had mild symptoms and mild reflux compared with weight lifters. In support, Peters and
colleagues [10] showed that although distance runners are prone to acid reflux,
lower GI symptoms, such as the urge to defecate and development of diarrhea,
are more prevalent (71%) than upper GI symptoms (36%). Cyclists exhibited
varying degrees of upper (67%) and lower (64%) GI symptoms, and triathletes
conformed to the patterns of GI distress during running and cycling.
Athletes who have exercise-related GERD may present with several symptoms that include substernal chest pressure, pain or burning that may mimic
angina, sour taste, intermittent water brash, globus hystericus, eructation,
nausea, and vomiting. A subset of athletes may present with atypical cough,
hoarseness, and wheezing—symptoms that mimic either exercise-induced bronchospasm (EIB) or vocal cord dysfunction.
There is good success in treating GERD with either lifestyle modifications,
medications, or both. Effective lifestyle modifications are a potent first-line
treatment in athletes who have GERD. These include avoidance of laying
down to sleep within 4 hours of the evening meal, postprandial exercise, and
excessive consumption of foods that relax the LES, including chocolate, peppermint, onions, high-fat foods, alcohol, tobacco, coffee, and citrus products.
Furthermore, sleeping on two pillows to enhance gravity-associated esophageal
clearance reduces the symptoms of GERD. And finally, athletes treated with
calcium-channel blockers for either migraine prophylaxis or control of hypertension should be counseled on the propensity for these drugs to reduce LES
pressure and worsen GERD.
Medications used to treat GERD include H2-receptor antagonists, proton
pump inhibitors (PPIs), and promotility agents. Although PPIs are effective in
treating GERD and endoscopic negative reflux disease (ENRD) [37], and have
been shown to be therapeutically superior to H2-receptor antagonists [37–40],
the literature on the efficacy of medications used to treat GERD in athletes
is sparse. In a single-blind, crossover study, Kraus and colleagues [33] showed
that markers of exercise-induced gastroesophageal reflux—percentage reflux
time and number of reflux episodes—can be reduced by pretreatment with
an H2-receptor antagonist (300 mg ranitidine) 1 hour prior to running. Van
Nieuwenhoven and colleagues [8] reported no significant changes in either percentage reflux time or number of reflux episodes between asymptomatic and
symptomatic cyclists exercising at 70% of VO2max. However, there was a higher
number and increased duration of reflux episodes in symptomatic individuals.
Therefore, a future double-blind, randomized control study to compare the effects of acid suppression on exercise-induced gastroesophageal reflux should
include asymptomatic and symptomatic athletes.
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There are good results managing GERD with PPIs as first-line treatment.
For persistent symptoms, the addition of a motility-influencing agent such
as dicyclomine may be effective. Athletes frequently eat shortly before bedtime,
a deleterious habit that can enhance postprandial reflux. Dicyclomine, in turn,
has been shown to decrease early postprandial reflux episodes [41]. Furthermore, success with the use of dicyclomine in a subset of athletes lends support
to the theory [8] that symptomatic athletes may indeed have a higher number of
LES relaxations during exercise. Finally, gastroesophageal reflux can provoke
or exacerbate EIB by either silent aspiration into the tracheobronchial tree or by
stimulating an acid-mediated esophagobronchial reflex [42,43]. The investigators have thus used treatment with PPIs in a subset of athletes afflicted with
GERD and EIB and noticed that it reduces symptoms of EIB.
DYSPEPSIA
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 for dyspepsia include peptic ulcer disease, GERD, and gastritis. Other
less common causes in this population include diabetes, thyroid disease, and
lactose intolerance.
Regardless of the cause of dyspepsia, the common clinical feature is mucosal
damage of the upper GI tract. As discussed elsewhere, gut mucosal injury occurs commonly in athletes secondary to complex physiologic adaptations that
deplete gut blood flow during exercise [8,10–13]. As a result, mucosal ischemia
depletes cellular ATP, expedites cell death, and induces mucosal inflammation
[44]. Frequent dehydration, repeated stress of competition, and excessive use
of NSAIDs, medications, alcohol, caffeine products, and dietary supplements
containing amino acids and creatine may further exacerbate mucosal injury and
eventually lead to blood loss and anemia.
Dyspepsia in athletes is easily preventable. However, dyspeptic symptoms
are vague, and athletes frequently delay assessment and treatment. Lifestyle
modifications akin to those used to treat GERD and avoidance of NSAIDs,
caffeine, tobacco, gas-producing foods (eg, broccoli, beans, eggs [30]), and dairy
products in athletes who have lactose intolerance generally helps alleviate
dyspeptic symptoms. Rehydration with carbohydrate drinks during exercise
may lessen mucosal damage by enhancing blood flow to absorption sites in the
gut, thereby reducing dyspepsia [45].
Failure of conservative therapy warrants testing and treatment for Helicobacter
pylori infection, especially in athletes who are from underdeveloped countries.
Although eradication of H pylori does not have significant effects on gastroesophageal acid reflux in patients who have established GERD, symptoms
of regurgitation have been shown to improve [46]. Therefore, a trial of either
PPI or H2-receptor antagonists may be useful in conjunction with appropriate
antibiotic therapy if the patient is H pylori-positive. Specialist referral and
esophagogastroduodenoscopy (EGD) are warranted in the presence of
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“alarm” symptoms and signs, such as odynophagia, dysphagia, hematochezia,
melena, anemia, positive fecal occult bleeding, loss of appetite, and unexplained
weight loss.
MOTILITY DISORDERS
Diarrhea
Distance runners and female athletes are most susceptible to lower intestinal
motility disorders that include diarrhea [47,48] and irritable bowel syndrome
(IBS) [8,10]. Although several theories have been proposed and a few studies
have elucidated mechanisms, the literature is limited and the precise pathophysiology remains largely undefined in the athletic population. Possible causative
factors include enteric fluid and electrolyte imbalance, mesenteric ischemia
contributing to increased mucosal permeability [14], mechanical trauma [47],
and altered colonic motility.
The data regarding the effects of exercise on colonic motility are varied.
Although aberrant small intestine activity has been shown during exercise
[4], physical activity does not have a well-defined effect on total transit time
through the GI tract [25]. Some studies have shown that, by independent
mechanisms, exercise can accelerate gut transit time of chyme and fecal residues
[5] and intraluminal gas [26]. The transit of chyme and fecal residues is largely a
passive process dependent on phasic motor activity and altered by exercise [49],
whereas the transit of gas is influenced by visceral reflexes and involves contraction/relaxation of the abdominal wall [50,51]. Furthermore, running has
been shown to delay small bowel transit time [1,8] and accelerate colonic transit
time [8]. Other studies, however, have found that exercise does not alter small
bowel or colonic motility [52], and transit time does not appear to be influenced
by short bouts of high-intensity exercise and is independent of the mechanical
bouncing of abdominal contents [53].
Fortunately, acute exercise-induced diarrhea, also known as “runner’s trots,”
is considered physiologic diarrhea that does not result in dehydration or
electrolyte imbalances and tends to improve with fitness level [1]. The diarrhea is defined as abnormally frequent, semisolid to watery bowel movements
(>
>3 times per day) that can be acute (<
<4 weeks) or chronic (>
>4 weeks).
In healthy athletes, acute diarrhea is either induced by running, food poisoning, traveler’s diarrhea, or viral gastroenteritis [54]. Typically, the diarrhea is
self-limited. In the absence of complications, such as fluid or electrolyte imbalance, protracted vomiting, melena, hematochezia, or frank bleeding per rectum,
supportive management with intravenous fluids, rest, and bismuth is sufficient. Athletes who have viral gastroenteritis should temporarily be excluded
from exposure to other teammates [54]. Avoidance of caffeine, NSAIDs, concentrated carbohydrate beverages, and foods with a high-glycemic index are
also effective therapeutic interventions [30]. Antidiarrheal medications such as
loperamide have adverse, depressive effects on the central nervous system, can
affect heat dissipation and concentration [30], and should be used with caution.
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CASEY, MISTRY, MACKNIGHT
Persistent diarrhea warrants a detailed workup to differentiate less serious
causes from more severe infective and chronic causes. Although uncommonly
encountered in athletes, infectious diarrhea must be ruled out if general supportive measures are inadequate. A history of a recent camping trip or wellwater consumption could be suggestive of giardiasis. Athletes who have sickle
cell trait or disease could have bloody diarrhea secondary to invasion with
salmonella. Diarrhea associated with right lower quadrant abdominal pain that
mimics appendicitis could be caused by Yersinia enterocolitica, and a history of
bloody diarrhea following recent consumption of poorly cooked beef could
suggest infection with hemorrhagic Escherichia coli (O157:H7). It is imperative to
obtain stool cultures prior to instituting specific therapy because generic treatment with ciprofloxacin can prolong salmonella infection and increase the risk
for hemolytic uremic syndrome in individuals who have hemorrhagic E coli
infection. Bloody diarrhea without an infectious cause, following the recent use
of antibiotics, and associated with abdominal pain and fever is highly suggestive
of Clostridium difficile colitis and should be aggressively treated with appropriate
antibiotic therapy.
Chronic diarrhea in young athletes could be secondary to medications (eg,
laxative abuse, antibiotics), lactose intolerance, malabsorption, irritable bowel
syndrome, hyperthyroidism, or inflammatory bowel disease (IBD). A stool
osmolar gap readily distinguishes secretory diarrhea from osmotic diarrhea
and is an especially pivotal component of the laboratory investigation for
chronic diarrhea in a female athlete at risk for an eating disorder. Indications
for specialist referral include chronic diarrhea secondary to malabsorptive
syndromes, such as sprue, Whipple’s disease, and IBD.
Irritable Bowel Syndrome
A functional GI disorder that is devoid of either structural, biomechanical,
radiologic or laboratory abnormalities, IBS affects up to 15% of the population
[55]. Two forms have been described: “diarrhea-predominant” and “constipation-predominant.” IBS is twice as common in women and typically presents
in the second or third decade of life. Approximately 50% of patients who have
IBS have comorbid psychiatric illnesses, including depression and anxiety.
Proposed mechanisms include increased motor reactivity to various stimuli, including stress, food, cholecystokinin, impaired transit of bowel gas [56,57],
visceral hypersensitivity, impaired reflex control that delays gas transit [58],
autonomic dysfunction, and altered immune activation [59].
The clinical characteristics are diverse, yet the most common symptoms
include cramping abdominal pain relieved by defecation, altered stool frequency, altered stool form (mucus, watery, hard, or loose), altered stool passage
(strain, urgency), a sense of incomplete evacuation, and abdominal distension
especially following meals. Athletes who have IBS rarely have nocturnal symptoms and do not manifest systemic signs of illness or hematochezia. The
differential diagnosis for IBS includes IBD, diarrhea secondary to sprue or
lactose intolerance, thyroid dysfunction, laxative abuse, diabetes, and psychia-
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tric illnesses. Current evidence does not support the routine use of laboratory
studies and imaging to exclude organic GI disorders in patients who have
typical IBS symptoms and are lacking “alarm” features [55].
Various lifestyle and dietary modifications are effective in treating IBS.
Reassurance, stress reduction, consumption of small meals during the day,
high-fiber diet, and avoidance of foods such as those containing lactose and
candy that contains sorbitol are helpful first-line measures. The role of regular
exercise in treating IBS has been studied in sedentary individuals who have IBS,
and has been shown to be a fairly effective treatment modality [60].
Drug treatment of IBS is based on the athletes’ predominant symptoms.
For diarrhea-predominant IBS, antidiarrheal (loperamide), antispasmodic (dicyclomine), and the 5-HT(3) receptor antagonist alosetron are efficacious.
Loperamide does inhibit the absorption of various drugs, including warfarin,
tetracyclines, NSAIDs, and thyroxine and should be used with extreme caution
in athletes who have hepatic insufficiency secondary to mononucleosis. Alosteron is currently only approved for treatment of severe, chronic IBS. In a
subset of patients who have diarrhea-predominant IBS and abdominal pain,
tricyclic antidepressants such as amitriptyline are effective. For constipationpredominant IBS, fiber, bulk laxatives and stool softeners are used, but their
efficacy is variable and may worsen symptoms. The 5-HT(4) receptor agonist
tegaserod may be efficacious, but is approved only for women who have
constipation-predominant IBS. Finally, the efficacy of psychologic counseling
is, at best, doubtful [61].
GASTROINTESTINAL BLEEDING
The occurrence of exercise-induced GI bleeding has been well documented,
particularly in distance runners [2,62–69]. Postexercise endoscopic colonic mucosal biopsy samples have revealed congestive and hemorrhagic vascular lesions [70,71]. Fortunately, GI bleeding following exercise is usually transient
and occult; however, there are case reports documenting substantial upper and
lower tract bleeds [5,63,66,72]. Ischemic colitis has been postulated to be a major
cause of GI bleeding during and after intense exercise [73]. As blood is shunted
from the viscera to the working muscles during maximal exercise, splanchnic
blood flow is decreased by as much as 80% [74]. Postcompetition studies have
supported this theory, as evidenced by the presence of endoscopic lesions
consistent with transient ischemic damage caused by decreased blood flow
with exercise [71]. Other proposed causes of exercise-induced GI bleeding
include hemorrhagic colitis [72] or gastritis secondary to the frequent use of
NSAIDs [62,75,76].
Other proposed mechanisms include hematuria [63], traumatic hemolysis [77],
impaired gut absorption [8], iron loss in sweat [78], decreased iron absorption
[79], poor dietary iron intake [79], and mechanical trauma [8] to the gut during
running. The lower incidence of occult bleeding in cyclists and the absence of
occult blood in walkers [62] support the theory that mechanical trauma to the gut
from frequent jostling in runners contributes to occult blood loss. As a group,
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runners have been shown to have lower ferritin, serum iron, and haptoglobin.
The frequency of iron deficiency is related to the distance and the intensity of
running [65]. 85% of ultramarathoners (100 miles) and triathletes [65] have been
found to have occult blood positivity. It is more prevalent in younger athletes
who have quicker times, and is more common during competition.
The differential diagnosis for GI bleeding is extensive, yet in young, healthy
athletes the most common causes should be excluded prior to an extensive
clinical investigation. GI bleeding is frequently occult and athletes typically
present with dyspnea on exertion, fatigue, and decreased endurance and
strength—anemic symptoms that may be compounded in female athletes who
have heavier than usual menstrual cycles. Although hematemesis is rare in this
population, prolonged retching can produce an esophageal “Mallory-Weiss”
tear in the esophagus. Diarrhea associated with bright red blood per rectum
or hematochezia warrants further workup for potentially serious conditions
such as ulcerative colitis and Crohn’s disease. Other common causes of lower
GI bleeding in athletes include hemorrhoids and anal fissures caused by frequent straining during defecation, especially in a subset of athletes who have
chronic constipation.
Early recognition and diagnosis of occult bleeding is critical to prevention of
poor athletic performance. Recommendations have been made for endoscopy
prior to instituting therapy for GI symptoms and anemia in runners [71].
However, the investigators have had good success in managing anemia using
a graded approach prior to routine endoscopy. Athletes who have fatigue, poor
performance, and decreased ferritin are treated with iron supplementation
containing at least 180 mg of elemental iron [69]. The investigators also counsel
athletes on prophylactic measures, such as optimizing dietary fiber intake,
maintaining optimal hydration that may decrease exercise-induced GI ischemia
[80], discontinuing the regular use of NSAIDs [75,76], and, in individuals who
have constipation and hemorrhoids, using stool softeners. The investigators do
not use H2 receptor blockers on a routine basis. The data on the prophylactic
use of H2 blockers (cimetidine) are varied [66,81–83], and only a subset of
athletes may have reduced occult blood loss following the use of cimetidine prior to competition [66,68]. Failure to respond to these initial measures,
despite normalization of ferritin, necessitates further clinical investigation and
specialist referral to rule out other causes of iron deficiency anemia.
Specialist referral and diligent monitoring of various medications are critical to optimal health and athletic performance in athletes who have IBD. Current literature contains conflicting data regarding the effect of intense athletic
participation in patients who have IBD. The general consensus suggests that
light and moderate exercise is well tolerated and can benefit patients who have
IBD [2]. Moreover, physical activity can counteract some of the adverse effects
of medications used to treat IBD, such as steroid-induced muscle weakness and
osteoporosis. Unfortunately, gut ischemia may exacerbate GI bleeding in
athletes who have IBD. Therefore, a safe guideline to follow is to ensure
hemodynamic stability prior to practice and competition [30].
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ABDOMINAL PAIN
Several self-limited GI illnesses in athletes present with abdominal pain, and
although the cause is diverse, early differentiation of emergent, surgical causes
from the more benign illnesses is of paramount importance. Mesenteric lymphadenitis, Meckel’s diverticulitis, strangulated inguinal hernia, ruptured ovarian
cyst, ectopic pregnancy, acute salpingitis, acute cystitis, pelvic inflammatory
disease, and endometriosis can all mimic acute appendicitis [84]. Abdominal
pain, anorexia, nausea, vomiting, and fever are common symptoms, but a
detailed history and clinical examination in the training room can determine
if the athlete who has abdominal pain needs an emergent surgical consult. A
history of recent respiratory tract or GI illness can cause mesenteric lymphadenitis. A tender palpable mass with overlying skin discoloration in the lower
quadrant is suggestive of incarcerated inguinal hernia. Acute, sharp abdominal
pain with nausea and vomiting during fixed times of the menstrual cycle can be
either secondary to a ruptured ovarian cyst or endometriosis. Abdominal pain
associated with hematuria and dysuria could be secondary to cystitis. Bilateral
lower quadrant pain with vaginal discharge, immediately following menses, is
typically caused by pelvic inflammatory disease. Finally, several medications
can reduce the efficacy of oral contraceptives and therefore, acute, unilateral
abdominal pain associated with hypotension and tachycardia could represent
ectopic pregnancy.
Acute appendicitis typically presents with constant, progressive, shifting pain.
The pain usually begins in the periumbilical area and subsequently moves to
the right lower quadrant over several hours. Additionally, anorexia, nausea,
vomiting, and fever are delayed symptoms that seldom precede the onset of
pain. Although acute appendicitis is overwhelmingly more common, chronic
appendicitis presenting as low back pain has been described in an athlete [85].
Appendicitis has also rarely been described following trauma to the abdominal
wall [86]. And finally, a rare case of marked psoas hypertrophy in a bodybuilder has been shown to mimic appendicitis secondary to compression of the
cecum [87].
Chronic abdominal pain in athletes in the absence of other constitutional
GI symptoms is most commonly caused by hernias. Hiatal hernia [88,89]
and umbilical and inguinal hernias have been described secondary to intraabdominal pressure overload [88,90]. Weakness of the musculotendinous part
of the posterior inguinal wall (“sportsmans’ hernia”) is also a common cause of
groin pain in athletes [91–93]. Surgical correction is indicated for persistent
symptoms [94–96] and laparoscopic hernioplasty is superior to conventional
herniorrhaphy [97].
MISCELLANEOUS GASTROINTESTINAL DISORDERS
Travel
Although only a few GI illnesses are associated with travel, athletes are particularly susceptible to acute gastroenteritis from bacterial [98] and viral [54] causes.
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CASEY, MISTRY, MACKNIGHT
Acute gastroenteritis typically presents with fever, nausea, vomiting, diarrhea,
cramping, and myalgias. There have been reports of acute outbreaks of gastroenteritis in the athletic population including Salmonella enteritidis at the Junior
World Rowing Championships at Poznan, Poland, in August 1995 [98], and
Norwalk viral gastroenteritis in a football team in the United States [99]. Athletes
who have acute gastroenteritis, especially those involved in contact sports,
should be prevented from participating in practices and competition until they
have been adequately treated, are afebrile, and are hemodynamically stable. And
in order to prevent contamination and spread, the fundamental importance of
good hygiene cannot be overemphasized.
Immunizations
Infectious hepatitis is common worldwide. Viral hepatitis, although rarely encountered in athletes, can be a significant source of morbidity. Outbreaks of
hepatitis A have been documented in soccer and football players [100]. Athletes
traveling to underdeveloped countries should receive the hepatitis A vaccination, with a booster at 6 months to ensure lifelong immunity. Unlike hepatitis A,
which is transmitted by way of the fecal–oral route, hepatitis B is transmitted
through blood-borne contamination. Transmission of hepatitis B between an
infected and a healthy athlete generally requires sustained contact between an
exposed skin or mucous membrane lesion—a situation that fortunately rarely
arises [100]. Nevertheless, hepatitis B vaccination is recommended for all athletes, especially those who participate in contact sports [101]. A three-dose series
of vaccinations over a 6-month period provides the most efficacious long-term
immunity. However, an accelerated series of vaccines can be administered over
2 months for athletes in need of emergent protection [101].
SUMMARY
Various physiologic adaptations to high-intensity exercise predispose athletes
to several common GI disorders. Although the potential mechanisms involved in
this increased susceptibility have been identified, few studies have compared GI
disorders between sedentary individuals and high-performance athletes. A clear
understanding of these mechanisms is pivotal for medical professionals charged
with the daily care of athletes to help develop effective diagnostic, preventive,
and therapeutic algorithms.
References
[1] Moses FM. The effect of exercise on the gastrointestinal tract. Sports Med 1990;
9(3):159–72.
[2] Bi L, Triadafilopoulos G. Exercise and gastrointestinal function and disease: an evidencebased review of risks and benefits. Clin Gastroenterol Hepatol 2003;1(5):345–55.
[3] Leitzmann MF, Giovannucci EL, Rimm EB, et al. The relation of physical activity to risk for
symptomatic gallstone disease in men. Ann Intern Med 1998;128:417–25.
[4] Simren M. Physical activity and the gastrointestinal tract. Eur J Gastroenterol Hepatol
2002;14(10):1053–6.
[5] Peters HP, De Vries WR, Vanberge-Henegouwen GP, et al. Potential benefits and hazards
of physical activity and exercise on the gastrointestinal tract. Gut 2001;48(3):435–9.
SPORTS GASTROENTEROLOGY
537
[6] Rehrer NJ, Meijer GA. Biomechanical vibration of the abdominal region during running
and bicycling. J Sports Med Phys Fitness 1991;31(2):231–4.
[7] Rehrer NJ, Brouns F, Beckers EJ, et al. Physiological changes and gastro-intestinal
symptoms as a result of ultra-endurance running. Eur J Appl Physiol Occup Physiol
1992;64(1):1–8.
[8] Van Nieuwenhoven MA, Brouns F, Brummer RJ. Gastrointestinal profile of symptomatic
athletes at rest and during physical exercise. Eur J Appl Physiol 2004;91(4):429–34.
[9] 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.
[10] Peters HP, Bos M, Seebregts L, et al. Gastrointestinal symptoms in long-distance runners,
cyclists, and triathletes: prevalence, medication, and etiology. Am J Gastroenterol 1999;
94(6):1570–81.
[11] Brouns F, Beckers E. Is the gut an athletic organ? Digestion, absorption and exercise.
Sports Med 1993;15(4):242–57.
[12] Konturek S, Falser J, Obtulowicz W. Effect of exercise on gastrointestinal secretions.
J Appl Physiol 1973;34:324–8.
[13] Bulkley GB, Kvietys PR, Parks DA, et al. Relationship of blood flow and oxygen consumption to ischemic injury in the canine small intestine. Gastroenterology 1985;89:852–7.
[14] Pals KL, Chang RT, Ryan AJ, et al. Effect of running intensity on intestinal permeability.
J Appl Physiol 1997;82(2):571–6.
[15] Worobetz LJ, Gerrard DF. Effect of moderate exercise on esophageal function in
asymptomatic athletes. Am J Gastroenterol 1986;81(11):1048–51.
[16] Brouns F. Gastric emptying as a regulatory factor in fluid uptake. Int J Sports Med
1998;19(Suppl 2):S125–8.
[17] Leiper JB, Broad NP, Maughan RJ. Effect of intermittent high-intensity exercise on gastri
emptying in man. Med Sci Sports Exerc 2001;33(8):1270–8.
[18] Rehrer NJ, Beckers EJ, Brouns F, et al. Effects of dehydration on gastric emptying and
gastrointestinal distress while running. Med Sci Sports Exerc 1990;22(6):790–5.
[19] Rehrer NJ, Beckers E, Brouns F, et al. Exercise and training effects on gastric emptying of
carbohydrate beverages. Med Sci Sports Exerc 1989;21(5):540–9.
[20] Van Nieuwenhoven MA, Vriens BE, Brummer RJ, et al. Effect of dehydration on
gastrointestinal function at rest and during exercise in humans. Eur J Appl Physiol 2000;
83:578–84.
[21] Russek M, Soto-Mora LM, Uriostegui T, et al. Effects of catecholamines on water intake in
rats. Physiol Behav 1991;49(1):201–6.
[22] Maresh CM, Gabaree-Boulant CL, Armstrong LE, et al. Effect of hydration status on thirst,
drinking, and related hormonal responses during low-intensity exercise in the heat. J Appl
Physiol 2004;97(1):39–44.
[23] Rehrer NJ, Brouns F, Beckers EJ, et al. Gastric emptying with repeated drinking during
running and bicycling. Int J Sports Med 1990;11(3):238–43.
[24] Rehrer NJ, van Kemenade M, Meester W, et al. Gastrointestinal complaints in relation to
dietary intake in triathletes. Int J Sport Nutr 1992;2(1):48–59.
[25] Soffer EE, Summers RW, Gisolfi C. Effect of exercise on intestinal motility and transit in
trained athletes. Am J Physiol 1991;260(5 Pt 1):G698–702.
[26] Dainese R, Serra J, Azpiroz F, et al. Effects of physical activity on intestinal gas transit and
evacuation in healthy subjects. Am J Med 2004;116(8):536–9.
[27] Castell DO, Donner MW. Evaluation of dysphagia: a careful history is crucial. Dysphagia
1987;2(2):65–71.
[28] DeGowin RL. DeGowin & DeGowin's bedside diagnostic examination. 5th edition. New
York: Macmillan Publishing Company; 1987.
[29] Soffer EE, Merchant RK, Duethman G, et al. Effect of graded exercise on esophageal motility and gastroesophageal reflux in trained athletes. Dig Dis Sci 1993;38(2):
220–4.
[30] Putukian M, Potera C. Don't miss gastrointestinal disorders in athletes. The Physician
538
[31]
[32]
[33]
[34]
[35]
[36]
[37]
[38]
[39]
[40]
[41]
[42]
[43]
[44]
[45]
[46]
[47]
[48]
[49]
[50]
[51]
[52]
CASEY, MISTRY, MACKNIGHT
and Sportsmedicine 1997;25(11). Available at http://physsportsmed.com. Accessed
June 14, 2005.
Shawdon A. Gastro-oesophageal reflux and exercise. Important pathology to consider in
the athletic population. Sports Med 1995;20(2):109–16.
Collings KL, Pierce Pratt F, Rodriguez-Stanley S, et al. Esophageal reflux in conditioned
runners, cyclists, and weightlifters. Med Sci Sports Exerc 2003;35(5):730–5.
Kraus BB, Sinclair JW, Castell DO. Gastroesophageal reflux in runners. Characteristics
and treatment. Ann Intern Med 1990;112(6):429–33.
Clark CS, Kraus BB, Sinclair J, et al. Gastroesophageal reflux induced by exercise in
healthy volunteers. JAMA 1989;261:3599–601.
Yazaki E, Shawdon A, Beasley I, et al. The effect of different types of exercise on gastrooesophageal reflux. Aust J Sci Med Sport 1996;28:93–6.
Peters HP, De Kort AF, Van Krevelen H, et al. The effect of omeprazole on gastrooesophageal reflux and symptoms during strenuous exercise. Aliment Pharmacol Ther
1999;13(8):1015–22.
van Pinxteren B, Numans ME, Bonis PA, et al. Short-term treatment with proton pump
inhibitors, H2-receptor antagonists and prokinetics for gastro-oesophageal reflux diseaselike symptoms and endoscopy negative reflux disease. Cochrane Database Syst Rev
2004;2(4):CD002095.
Chiba N, De Gara CJ, Wilkinson JM, et al. Speed of healing and symptom relief in
grade II to IV gastroesophageal reflux disease: a meta-analysis. Gastroenterology 1997;
112(6):1798–810.
Beck IT, Champion MC, Lemire S, et al. The Second Canadian Consensus Conference on
the Management of Patients with Gastroesophageal Reflux Disease. Can J Gastroenterol
1997;(11 Suppl B):7B–20B.
Carlsson R, Galmiche JP, Dent J, et al. Prognostic factors influencing relapse of
oesophagitis during maintenance therapy with antisecretory drugs: a meta-analysis of
long-term omeprazole trials. Aliment Pharmacol Ther 1997;11(3):473–82.
Koerselman J, Pursnani KG, Peghini P, et al. Different effects of an oral anticholinergic
drug on gastroesophageal reflux in upright and supine position in normal, ambulant
subjects: a pilot study. Am J Gastroenterol 1999;94(4):925–30.
Boyle JT. Pathogenic gastroesophageal reflux in infants and children. Practical
Gastroenterology 1990;14:25–38.
Mathew JL, Singh M, Mittal SK. Gastro-oesophageal reflux and bronchial asthma: current
status and future directions. Postgrad Med J 2004;80(950):701–5.
Oktedalen O, Lunde OC, Opstad PK, et al. Changes in gastrointestinal mucosa after longdistance running. Scand J Gastroenterol 1992;27:270–4.
Haglund U. Gut ischemia. Gut 1994;35(Suppl 1):S73–6.
Guliter S, Kandilci U. The effect of Helicobacter pylori eradication on gastroesophageal
reflux disease. J Clin Gastroenterol 2004;38(9):750–5.
Butcher JD. Runner's diarrhea and other intestinal problems of athletes. Am Fam Physician
1993;48(4):623–7.
Sullivan SN, Wong C. Runners diarrhea. Different patterns and associated factors. J Clin
Gastroenterol 1992;14(2):101–4.
Rao SS, Beaty J, Chamberlain M, et al. Effects of acute graded exercise on human colonic
motility. Am J Physiol 1999;276(5 Pt 1):G1221–6.
Serra J, Azpiroz F, Malagelada JR. Gastric distension and duodenal lipid infusion
modulate intestinal gas transit and tolerance in humans. Am J Gastroenterol 2002;
97(9):2225–30.
Harder H, Serra J, Azpiroz F, et al. Reflex control of intestinal gas dynamics and tolerance
in humans. Am J Physiol Gastrointest Liver Physiol 2004;286(1):G89–94.
Rao KA, Yazaki E, Evans DF, et al. Objective evaluation of small bowel and colonic transit
time using pH telemetry in athletes with gastrointestinal symptoms. Br J Sports Med 2004;
38(4):482–7.
SPORTS GASTROENTEROLOGY
539
[53] Kayaleh RA, Meshkinpour H, Avinashi A, et al. Effect of exercise on mouth-to-cecum
transit in trained athletes: a case against the role of runners' abdominal bouncing.
J Sports Med Phys Fitness 1996;36(4):271–4.
[54] Becker KM, Moe CL, Southwick KL, et al. Transmission of Norwalk virus during a football
game. N Engl J Med 2000;343:1223–7.
[55] Cash BD, Chey WD. Irritable bowel syndrome - an evidence-based approach to
diagnosis. Aliment Pharmacol Ther 2004;19(12):1235–45.
[56] Caldarella MP, Serra J, Azpiroz F, et al. Prokinetic effects in patients with intestinal gas
retention. Gastroenterology 2002;122(7):1748–55.
[57] Serra J, Azpiroz F, Malagelada JR. Impaired transit and tolerance of intestinal gas in the
irritable bowel syndrome. Gut 2001;48(1):14–9.
[58] Serra J, Salvioli B, Azpiroz F, et al. Lipid-induced intestinal gas retention in irritable bowel
syndrome. Gastroenterology 2002;123(3):700–6.
[59] Lin HC. Small intestinal bacterial overgrowth: a framework for understanding irritable
bowel syndrome. JAMA 2004;292(7):852–8.
[60] Lustyk MK, Jarrett ME, Bennett JC, et al. Does a physically active lifestyle improve
symptoms in women with irritable bowel syndrome? Gastroenterol Nurs 2001;24(3):
129–37.
[61] Cremonini F, Talley NJ. Diagnostic and therapeutic strategies in the irritable bowel
syndrome. Minerva Med 2004;95(5):427–41.
[62] Robertson JD, Maughan RJ, Davidson RJ. Fecal blood loss in response to exercise. Br Med
J (Clin Res Ed) 1987;295(6593):303–5.
[63] Halvorsen FA, Lyng J, Ritland S. Gastrointestinal bleeding in runners. Scand J
Gastroenterol 1986;21(4):493–7.
[64] Babic Z, Papa B, Sikirika-Bosnjakovic M, et al. Occult gastrointestinal bleeding in rugby
player. J Sports Med Phys Fitness 2001;41(3):399–402.
[65] Rudzki SJ, Hazard H, Collinson D. Gastrointestinal blood loss in triathletes: it's etiology
and relationship to sports anaemia. Aust J Sci Med Sport 1995;27(1):3–8.
[66] Moses FM. Gastrointestinal bleeding and the athlete. Am J Gastroenterol 1993;88(8):
1157–9.
[67] Baska RS, Moses FM, Graeber G, et al. Gastrointestinal bleeding during an
ultramarathon. Dig Dis Sci 1990;35(2):276–9.
[68] Baska RS, Moses FM, Deuster PA. Cimetidine reduces running-associated gastrointestinal
bleeding. A prospective observation. Dig Dis Sci 1990;35(8):956–60.
[69] Nickerson HJ, Holubets MC, Weiler BR, et al. Causes of iron deficiency in adolescent
athletes. J Pediatr 1989;114(4 Pt 1):657–63.
[70] Gaudin C, Zerath E, Guezennec CY. Gastric lesions secondary to long-distance running.
Dig Dis Sci 1990;35(10):1239–43.
[71] Choi SC, Choi SJ, Kim JA, et al. The role of gastrointestinal endoscopy in longdistance runners with gastrointestinal symptoms. Eur J Gastroenterol Hepatol 2001;13(9):
1089–94.
[72] Moses FM, Brewer TG, Peura DA. Running-associated proximal hemorrhagic colitis.
Ann Intern Med 1988;108:385–6.
[73] Heer M, Repond F, Hany A, et al. Acute ischaemic colitis in a female long-distance runner.
Gut 1987;28:986–9.
[74] Qumar M, Read A. Effects of mesenteric blood flow in man. Gut 1987;28:583–7.
[75] Davies NM, Saleh JY, Skjodt NM. Detection and prevention of NSAID-induced
enteropathy. J Pharm Pharm Sci 2000;3(1):137–55.
[76] Davies NM, Wallace JL. Nonsteroidal anti-inflammatory drug-induced gastrointestinal
toxicity: new insights into an old problem. J Gastroenterol 1997;32(1):127–33.
[77] Radomski MW, Sabiston BH, Isoard P. Development of sports anemia in physically fit men
after daily sustained submaximal exercise. Aviat Space Environ Med 1980;51:41–5.
[78] Lamanca JJ, Haymes EM, Daly JA, et al. Sweat iron loss of male and female runners
during exercise. Int J Sports Med 1988;9:52–5.
540
CASEY, MISTRY, MACKNIGHT
[79] Clement DB, Asmundson RC. Nutritional intake and hematological parameters in
endurance runners. Phys Sportsmed 1982;10:37–43.
[80] Peters HP, Akkermans LM, Bol E, et al. Gastrointestinal symptoms during exercise. The
effect of fluid supplementation. Sports Med 1995;20:65–76.
[81] Montgomery LC, Deuster PA. Effects of antihistamine medications on exercise
performance. Implications for sportspeople. Sports Med 1993;15(3):179–95.
[82] Moses FM, Baska RS, Peura DA, et al. Effect of cimetidine on marathon-associated
gastrointestinal symptoms and bleeding. Dig Dis Sci 1991;36(10):1390–4.
[83] Cooper BT, Douglas SA, Firth LA, et al. Erosive gastritis and gastrointestinal bleeding in a
female runner. Prevention of the bleeding and healing of the gastritis with H2-receptor
antagonists. Gastroenterology 1987;92(6):2019–23.
[84] Bergman RT. Assessing acute abdominal pain: a team physician's challenge. The
Physician and Sportsmedicine 1996;24(4). Available at http://physsportsmed.com.
Accessed June 14, 2005.
[85] Drezner JA, Harmon KG. Chronic appendicitis presenting as low back pain in a
recreational athlete. Clin J Sport Med 2002;12(3):184–6.
[86] Ramsook C. Traumatic appendicitis: fact or fiction? Pediatr Emerg Care 2001;17(4):
264–6.
[87] Zeiss J, Smith RR, Taha AM. Iliopsoas hypertrophy mimicking acute abdomen in a
bodybuilder. Gastrointest Radiol 1987;12(4):340–2.
[88] Dickerman RD, McConathy WJ, Smith AB. Can pressure overload cause sliding hiatal
hernia? A case report and review of the literature. J Clin Gastroenterol 1997;25(1):
352–3.
[89] Smith AB, Dickerman RD, McGuire CS, et al. Pressure-overload-induced sliding hiatal
hernia in power athletes. J Clin Gastroenterol 1999;28(4):352–4.
[90] Dickerman RD, Smith A, Stevens QE. Umbilical and bilateral inguinal hernias in a veteran
powerlifter: is it a pressure-overload syndrome? Clin J Sport Med 2004;14(2):95–6.
[91] Kemp S, Batt ME. The “Sports Hernia”: a common cause of groin pain. The Physician
and Sportsmedicine 1998;26(1). Available at http://physsportsmed.com. Accessed
June 14, 2005.
[92] LeBlanc KE, LeBlanc KA. Groin pain in athletes. Hernia 2003;7(2):68–71.
[93] Akita K, Niga S, Yamato Y, et al. Anatomic basis of chronic groin pain with special
reference to sports hernia. Surg Radiol Anat 1999;21(1):1–5.
[94] Malycha P, Lovell G. Inguinal surgery in athletes with chronic groin pain: the ‘sportsman's’
hernia. Aust N Z J Surg 1992;62(2):123–5.
[95] Taylor DC, Meyers WC, Moylan JA, et al. Abdominal musculature abnormalities as a
cause of groin pain in athletes. Inguinal hernias and pubalgia. Am J Sports Med 1991;
19(3):239–42.
[96] Srinivasan A, Schuricht A. Long-term follow-up of laparoscopic preperitoneal hernia
repair in professional athletes. J Laparoendosc Adv Surg Tech A 2002;12(2):101–6.
[97] Murata N, Ishida H, Makita Y, et al. Muscle strength and walking ability after
laparoscopic hernioplasty versus conventional repair. Surg Today 2003;33(4):259–63.
[98] Anderson AC. Outbreak of Salmonella food poisoning at Junior World Rowing
Championships. Br J Sports Med 1996;30(4):347–8.
[99] Becker KM, Moe CL, Southwick KL, et al. Transmission of Norwalk virus during football
game. N Engl J Med 2000;343(17):1223–7.
[100] Harrington DW. Viral hepatitis and exercise. Med Sci Sports Exerc 2000;32(7):
S422–30.
[101] Jimenez CE. Preparing active patients for international travel. The Physician and
Sportsmedicine 2003;31(10). Available at http://physsportsmed.com. Accessed
June 14, 2005.