Abstract
Relationships between peptic ulcer and physical activity have as yet received little attention. The prevalence of ulceration is high in racehorses and sled dogs, particularly during periods of competition. In humans, some occupational comparisons show an increased risk among manual workers, but it remains difficult to separate effects of work-related activity from social class and attendant influences of smoking, excessive alcohol consumption, shift work, and other stressors. Two studies of leisure activity point to some benefit from moderate physical activity, one finding a reduced risk of gastric ulcers and the other finding no effect on gastric ulcers but a reduced risk of duodenal ulcers in men only. Moderate physical activity could have a favorable impact on a number of risk factors for peptic ulceration. It could reduce gastric secretions and enhance immune function, with the latter reducing the risk of Helicobacter pylori infection. Moderate activity might also reduce anxiety and encourage the adoption of a healthy lifestyle, with avoidance of smoking and an excessive consumption of alcohol. However, prolonged endurance exercise seems likely to have a negative impact, suppressing immune function, reducing mucosal blood flow, and calling for frequent administration of non-steroidal anti-inflammatory drugs (NSAIDs). As with other aspects of exercise medicine, there may be a J-shaped relationship between dose and response. Limited human observations suggest a favourable response to bouts of moderate leisure activity but little benefit from heavy occupational activity and, in some animal studies, negative effects at high volumes and intensities of exercise. Further research is recommended to confirm the nature of this relationship, clarify the location of any nadir of risk for various classes of individual, and to explore mechanisms and antidotes.
Similar content being viewed by others
Limited human observations suggest that moderate leisure activity may reduce the risk of peptic ulcers, but, at least in animals such as racehorses, intensive competition is associated with a high prevalence of peptic ulceration. |
Potential factors modulating the risk of ulceration with regular moderate exercise include a decreased gastric acid secretion, enhanced immune function, a reduction of anxiety, and encouragement of a healthy lifestyle. |
There is a need to study athletes who engage in frequent and intensive competition to see if they show the increased risk of peptic ulceration observed in some animals. |
1 Introduction
A peptic ulcer is a break in the lining of the stomach, the duodenum or, occasionally, the oesophagus. Gastric and duodenal ulcers are relatively common and will be the focus of this review. Self-reports suggest that over a single year of observation, as many as 3 % of the population are affected [1], although prevalence seems to have decreased recently. One global literature review set the annual incidence of physician-diagnosed peptic ulcer as low as 0.10–0.19 % [2], and endoscopy of symptomless volunteers in Louisiana, USA, found that the prevalence of duodenal ulcers was 1.8 %, and 1.1 % for gastric ulcers [3, 4]. Ulceration is apparently associated with endogenous factors such as heredity, an excessive secretion of gastric acid and pepsin, and an impaired mucosal blood flow, as well as exogenous influences that include Helicobacter pylori infection, smoking, excessive alcohol consumption, stress, and overuse of non-steroidal anti-inflammatory drugs (NSAIDs) [5, 6]. However, both limitations of diagnosis and interactions between predisposing factors hamper determination of the dominant etiology [4].
The potential impact of habitual physical activity on peptic ulceration has as yet received little attention. Regular physical activity could conceivably reduce risk by modifying several of the factors noted above (Table 1), decreasing gastric acid secretion, enhancing mucosal blood flow, stimulating immune function and thus countering H. pylori infection, and diminishing stress and anxiety. An active lifestyle could also encourage the adoption of favorable health behaviors, with a low prevalence of smoking and excessive alcohol consumption. On the other hand, competitive athletes might increase their risks of ulceration through increased use of NSAIDs, immunosuppression, and the development of visceral ischaemia during bouts of intensive and prolonged exercise.
This brief review looks at empirical findings on exercise and peptic ulceration, and supplements this limited database by considering how physical activity might modify risk factors for peptic ulceration.
2 Empirical Data
Much of the empirical data concerning exercise and peptic ulcers have been collected on racehorses, sled dogs and laboratory animals. Such studies point consistently to an adverse effect of prolonged and vigorous physical activity, with an association between race participation and a high prevalence of ulceration. There have been a few cross-sectional human studies based on groups differing in occupational or leisure activity, and these provide some evidence that regular moderate exercise may reduce the risk of peptic ulceration. However, there do not seem to be any reports looking specifically at elite athletes; this would be an interesting question to investigate, in view of the high incidence of peptic ulceration in racehorses.
2.1 Animal Models
2.1.1 Horses
The prevalence of gastric ulcers in racehorses is very high. One French study found that, outside of the main racing season, 48 % of high-level endurance racehorses had gastric ulcers, and 93 % were affected at times of the year when the animals were competing frequently [7]. Other investigations in New Zealand, North America and Sweden have noted a similar high prevalence of peptic ulcers among racehorses [8–12]. Ulcers seem somewhat more frequent in trotters than in pacers [13] and, although the number of lesions decreases during detraining [14], a substantial prevalence remains [15], with an adverse effect on maximal oxygen consumption and other aspects of the animal’s physical performance [16].
Suggested mechanisms include a tensing of the abdominal muscles that pushes acidic gastric contents into the proximal stomach when galloping [17], exercise-induced increases in concentrations of gastrin and thus acid secretion [18], repeated administration of hypertonic electrolytes [19], and the stress of transport to and from sites of competition [20]. The importance of acid secretion to ulceration is suggested by the effectiveness of histamine receptor 2 (H2) antagonists [21, 22] and proton pump inhibitors [22–27] in treatment. Benefit has also been found from administration of sulcrafate, a combination of sucrose, sulphate and aluminium; this inhibits pepsin and increases prostaglandin levels, although the protection against ulceration probably derives mainly from an increased production of mucin [28].
2.1.2 Other Animals
Dogs that are involved in long-distance sled racing also seem very vulnerable to peptic ulcers [29, 30]. Races that can cover 160 km/day increase intestinal permeability [31], worsen ulceration [30], and sometimes lead to death during the event [32].
Excessive wheel running also causes peptic ulcers in laboratory rats. The likelihood of ulceration can be reduced by chemical ablation of the ventromedial hypothalamus [33]. The authors of this report suggested that the ventromedial hypothalamus plays a crucial role in causing excessive running when rats are exposed to stress [33].
2.2 Occupational Activity
The choice of occupation may influence both habitual physical activity and stress levels, and it is often a determinant of socioeconomic status. The prevalence of peptic ulcers is high among night and shift workers, but here stress and irregular meals seem the main culprits [34, 35].
The classical observations of Doll et al. [36] showed a similar incidence of peptic ulcers in bus drivers and conductors (a comparison where socioeconomic status was comparable, but where there was a large intergroup difference in occupational activity). Both bus drivers and conductors had higher rates of ulceration than agricultural workers (who, in the era of the study by Doll et al., commonly had high average rates of energy expenditure).
Some early reports linked peptic ulcers to what were apparently sedentary tasks: professional employment, being a supervisor or holding a responsible position [36–39]; however, these results were not controlled for leisure activity or, in the case of air-traffic controllers [37], for the demands of shift work. A study from northern Norway [40] found a high prevalence of peptic ulcers in fishermen and land and sea transport workers; it was speculated that the stress of dangerous work, irregular hours and heavy smoking might be causal factors.
More recent data have found the highest rates of peptic ulcers in unskilled workers [41–44]. It has also been suggested that the high prevalence among migrant workers reflects their current predominance in physically demanding jobs, and that the secular decline in incidence of peptic ulcer may be linked to a progressive reduction in average energy expenditures at work [44].
The most recent analysis [45] found that even after adjusting for the covariates of age, smoking habits and social class, the risk of a recent diagnosis of duodenal ulcer was 1.3 for those who were engaged in moderate physical work, and 3.6 for individuals with a high level of occupational activity.
2.3 Leisure Activity
Chen et al. [46, 47] made a cross-sectional analysis of data for 8529 men and 2884 women attending the Cooper Fitness Center, Dallas, TX, USA. Participants were categorized as ‘active’ (those who reported walking or running >16 km/week), ‘moderately active’ (covering <16 km/week), or ‘inactive’. A proportional hazards model that made statistical adjustments for age, smoking, alcohol use, body mass index, and self-reported ‘tension’ found no impact of habitual physical activity on the incidence of physician-diagnosed gastric ulcers, but there were significant differences for duodenal ulcers in men only (relative hazards 0. 38 for active and 0.54 for moderately active relative to inactive individuals); this study made no specific allowance for socioeconomic status but, given the exclusive nature of the fitness center, most of the study participants were likely relatively wealthy individuals. In discussing the absence of influence of activity on duodenal ulcers in women, the authors of this report suggested that the activity patterns of the women may have differed from that of the men, both in type and intensity; they also noted that the power of the statistical analysis for the women was limited because only a very small number of females had peptic ulcers.
A random sampling of 2416 Danish adults used self-reports and a national registry to determine the incidence of peptic ulcer over a 12-year period. A multivariate logistic analysis of the data included the detection of Helicobacter antibodies, smoking, alcohol consumption, and the use of NSAIDs and gastrointestinal drugs, but not socioeconomic status. Participants classed themselves as sedentary, ambulatory or active, and inclusion of this variable in the analysis showed a significantly lower risk of gastric ulcer in those who described themselves as ambulatory rather than sedentary (odds ratio 0.4). However, benefit for those who classed themselves as active (0.70) was not significantly lower than that of sedentary individuals, and physical activity held no apparent advantage for those with duodenal ulcers [48].
3 Exercise and Endogenous Risk Factors
Of endogenous risk factors for peptic ulceration, both mucosal blood flow and gastric secretions can be modified by exercise. It has further been argued that local bicarbonate secretion is totally dependent on local blood flow.
3.1 Mucosal Blood Flow
Local circulation to the gastric mucosa is closely associated with both the pathogenesis and healing of peptic ulcers [49]. Among other functions, the local blood flow brings oxygen and bicarbonate ions, and removes excessive hydrogen ions [50]. Mucosal blood flow may be compromised either by an accumulation of the vasoconstrictor endothelin caused by the administration of NSAIDs (see Sect. 4.4) [51], or by the visceral ischaemia associated with prolonged endurance exercise [52]. With an extreme challenge, such as completion of an ultra-triathlon, the reduction of local blood flow can be severe enough to damage the integrity of the gastrointestinal endothelium, with plasma antibodies signalling the absorption of intestinal endotoxins [53]; however, an adverse effect on endothelial function is unlikely unless prolonged exercise is undertaken at an intensity >75 % of maximal oxygen intake. Regular moderate exercise should enhance the physical condition of an individual, thus lessening the likelihood that any given bout of vigorous physical activity will exceed the threshold fraction of maximal oxygen intake where endothelial function is compromised; however, protection will not be increased if the individual then exercises to a higher absolute intensity of effort.
3.2 Gastric Secretions
The amount of gastric acid that is secreted seems a factor in the genesis of, and particularly in the healing of, peptic ulcers, although the relationship is far from simple [54]. In horses, at least, acid secretion is increased by a starch diet [7], and ulceration is alleviated by H2 antagonists and proton pump inhibitors (see Sect. 2.1.1). In reviewing early human experiments, Sullivan suggested that investigations were often flawed by unphysiological methods for both the stimulation and measurement of gastric secretions [55–57]. Nevertheless, he reached the broad conclusion that moderate exercise had little effect on gastric secretions, whereas vigorous exercise decreased both basal acid output and acid secretion in response to food and histamine. Moreover, these effects were independent of vagal innervation, and cross-transfusion experiments suggested hormonal involvement [55]. Furthermore, the exercise-induced inhibition of acid secretion persisted into the recovery period [58, 59], was inversely related to fitness level, and was exacerbated by competition [60].
More recent studies of this issue have been inconsistent, with some authors finding reductions in basic acid secretion and the secretory response to 5 % glucose during or following exercise [58, 59, 61, 62], and others seeing no change with exercise to 75 % of maximal aerobic power [63–65]. Two authors compared responses in healthy individuals and in those with peptic ulcers. Zach et al. [59] found that cycling at 50 % of maximal heart rate reduced the basal volume of gastric secretion and the hydrochloric acid concentration in both healthy individuals and those with gastric ulcers, but increased acid secretion in those with duodenal ulcers. Likewise, Canalles et al. [61] reported that exercise in the training zone decreased basal acid secretion in healthy individuals relative to a previous period of rest, but increased it in those with peptic ulcers.
Zach et al. [59] found that 1 h of cycle ergometer exercise at 50 % of the individual’s maximal heart rate not only reduced the volume of basal gastric secretion but also its electrolyte content. Oektedalen et al. [66] also noted a decrease in meal-stimulated gastrin secretion during an arduous 4-day military exercise. The secretion of gastrointestinal hormones (gastrin, motilin, glucagon, pancreatic polypeptide, and vasoactive intestinal peptide) seem unaffected by exercise at intensities up to 90 % of maximal oxygen intake (\(\dot{V{\text{O}}}\) 2max) [67, 68], although increases in the serum gastrin response to feeding have been observed in endurance racehorses following rigorous training [18]. Interval training also increases grehlin and leptin levels, at least in horses [69].
We may conclude that moderate exercise has either no effect or reduces gastric secretions in healthy individuals, but this is less clearly established for those with established lesions. There is no recent information on the effects of very vigorous exercise in humans, although associated lactate accumulation may decrease gastric mucosal pH [70].
4 Exercise and Exogenous Risk Factors
Of exogenous risk factors, exercise may modify H. pylori infections, smoking and alcohol consumption, stress, and the use of NSAIDs. Levels of habitual physical activity are also associated with socioeconomic status, another apparent risk factor for peptic ulceration.
4.1 Helicobacter pylori Infection
Helicobacter pylori was once thought to be the prime factor causing peptic ulcers and, indeed, one study found no relapses in patients where the microorganism was eliminated by antibiotic therapy [71]. However, more recent investigators have recognized that such infections occur in a large fraction of the world population, selectively affecting lower socioeconomic groups and confounding many of the studies of exercise and peptic ulceration.
Could exercise patterns modulate the risk of infection by this microorganism? There is good evidence that a bout of prolonged endurance exercise or a period of very vigorous training has at least a short-lived adverse effect on the immune system, increasing the risk of upper respiratory infections [72–74]. There is also less substantial evidence that regular moderate exercise has a beneficial effect, increasing salivary immunoglobulin A levels [75, 76] and reducing the risk of respiratory infections [77]. Moreover, levels of immunoglobulin A in saliva and gastric juice correlate with protection against H. pylori [78, 79]. However, direct proof of benefit from an action of moderate physical activity against H. pylori is difficult to establish from epidemiological research, because both the Helicobacter infection and habitual physical activity are linked to socioeconomic status, and it is difficult to find an index that will eliminate all of the resultant covariation from statistical analyses.
4.2 Cigarette Smoking and Alcohol Consumption
Cigarette smoking is associated with the development of gastric ulcers, and particularly duodenal ulcers [80], with adverse effects from an accumulation of free radicals, a decrease of mucosal nitric oxide synthase activity and resultant decreases in mucosal blood flow. Likewise, excessive consumption of alcohol is linked to gastric metaplasia, reduced mucosal integrity, an increased risk of H. pylori infection, and an increased likelihood of peptic ulceration [81]. However, again, there are problems of data interpretation since smoking and the abuse of alcohol are related to stress, anxiety and a low socioeconomic status.
Regular exercisers are usually non-smokers, and there is some evidence that exercise can help in smoking cessation programmes [82–85]. The association between excessive alcohol consumption and sport is less clear cut [85]; some athletic clubs consume large amounts of alcohol following a successful competition, and problem drinkers may also increase their physical activity in an attempt to avoid weight gain [86].
4.3 Stress and Anxiety
Stress and/or anxiety seem linked to peptic ulceration; the prevalence of ulcers increases threefold in those reporting stress [87] or tranquillizer use [48]. Stress could also increase other risk factors such as smoking and alcohol consumption; statistical analyses have controlled for reports of ‘current smoking’ [87], or cumulative tobacco consumption [48], but not for the number of cigarettes consumed in recent weeks.
Regular physical activity has a small but positive effect on anxiety level. One early study found that 20 min of exercise at 70 % of self-imposed maximal heart rate reduced state anxiety by an amount equal to 20 min of formal meditation [88], and a more recent survey of 159 reports concluded that trait anxiety was lower in fit individuals, and state anxiety could be reduced by aerobic exercise [89]. On the other hand, involvement in competitive exercise could substantially increase anxiety and stress.
4.4 Administration of Non-Steroidal Anti-Inflammatories
Empirical studies on the habitual use of NSAIDs and the risk of peptic ulcers have yielded conflicting results [90] but it seems likely that prostaglandin inhibition may compromise gastroduodenal defences, including local blood flow, mucus and bicarbonate secretion. Risks are thus likely to be increased in high-intensity exercisers who make frequent use of NSAIDs [91]. One US study found that 15 % of high-school football players were taking NSAIDs on a daily basis [92].
4.5 Socioeconomic status
A low socioeconomic status is commonly considered a risk factor for peptic ulceration, although this is, in part, because individuals with low status are more likely to face shift work and stress at work and at home, with a greater probability of smoking, an excessive consumption of alcohol, and H. pylori infection. Individuals with low socioeconomic status may still have a physically demanding job but from a young age their leisure activity is substantially lower than that of the upper echelons of society [93, 94].
5 Discussion
Given the prevalence of peptic ulcer in the general population, there has been surprisingly little study of the influence of habitual physical activity on either risk factors or on the optimal management of affected individuals. Studies in animals, particularly in racehorses, point towards a negative effect of prolonged and intensive exercise, although this inference must be tempered by difficulties in allowing for dietary change, the use of hypertonic fluids and medication, prolonged travel and other stressors associated with the participation of animals in high-level competition [19, 20].
In humans, occupational studies have yielded conflicting results, with more recent investigations pointing to a negative influence from physically demanding manual work. However, it has often been difficult to ensure a complete elimination of effects from covariates of the low socioeconomic status associated with manual work, such as an increased risk of H. pylori infection, a high prevalence of smoking and an excessive consumption of alcohol, and a greater likelihood of shift work. In a comparison of London Transport bus drivers and conductors, where socioeconomic status, shift work and canteen meals were comparable for the two groups of employees, no reduction of risk was associated with the much greater physical activity required from the conductors [36]. Given the increasing automation of most employment, further occupational studies seem unlikely to be fruitful.
It is remarkable that to date there have only been two studies of leisure activity and peptic ulceration [46–48]. One of these investigations was uncontrolled for socioeconomic status [48] and, although the subjects in both studies were classified into three levels of habitual activity, neither report was able to obtain a very precise description of the types and volumes of activity undertaken. Both investigations pointed towards benefit from engagement in regular moderate physical activity, although one found an effect on gastric ulcers and the other found no influence on gastric ulcers but a reduction of duodenal ulcers in men only.
There remains a need for further study of both recreational exercisers and athletes to clarify these discrepancies. However, as with other facets of health, a combination of leisure and occupational data for human subjects and observations on animals point toward a J-shaped relationship between exercise and benefit, with moderate leisure activity reducing the risks of ulceration, heavy occupational activity having little positive effect, and very vigorous activity increasing prevalence, at least in some animals. It is important for those managing peptic ulcers that possible adverse consequences of very vigorous exercise be evaluated further in human subjects and, if such an effect is confirmed, that the nadir of risk be established for those at various levels of initial physical condition.
There is also a need for further study of the mechanisms underlying any benefits from moderate exercise. The effects of administering proton inhibitors to racehorses point to a possible influence from a decrease in gastric acid secretion. Exercise may also be modulating immune function and thus H. pylori infection, although it is difficult to evaluate this question by epidemiological study and, in any event, exercise-induced changes of immune response are generally small and short-lived. Some benefit may come from exercise-induced relief of anxiety or improvement of lifestyle. Finally, regular physical activity will enhance physical condition, so that when a given heavy task must be accomplished it is less likely to demand a large fraction of maximal oxygen intake and thus predispose to ulceration.
6 Conclusions
A combination of animal and human research suggests that there may be a J-shaped relationship between habitual physical activity and the risk of peptic ulcer, with benefit from low to moderate levels of exercise, and an increased risk from intensive and prolonged physical activity; however, information is as yet limited. Further research is needed to determine whether very high intensities of effort are harmful to humans and, if so, to locate the nadir of risk.
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Shephard, R.J. Peptic Ulcer and Exercise. Sports Med 47, 33–40 (2017). https://doi.org/10.1007/s40279-016-0563-4
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DOI: https://doi.org/10.1007/s40279-016-0563-4