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Gut 2001;48:435–439
Potential benefits and hazards of physical activity and exerciseon the gastrointestinal tract The role of physical activity in the treatment of This review describes the current state of knowledge on the gastrointestinal diseases will not be discussed, as the litera- hazards of exercise and the potential benefits of physical ture on this topic is scarce. Nevertheless, in patients with activity on the gastrointestinal tract. In particular, acute gastrointestinal diseases physical activity may inhibit mus- strenuous exercise may provoke gastrointestinal symptoms cle loss, and improve appetite, functional capacity, and such as heartburn or diarrhoea. A substantial part general well being by positive mood changes5.
(20–50%) of endurance athletes are hampered by thesesymptoms which may deter them from participation intraining and competitive events. Nevertheless, these acute symptoms are transient and do not hamper the athlete’s Gastrointestinal symptoms such as nausea, heartburn, health in the long term. The only exception is repeated diarrhoea, and gastrointestinal bleeding are common dur- gastrointestinal bleeding during training and competition, ing exercise, especially during vigorous sports such as long which in the long term may occasionally lead to iron defi- distance running and triathlons.2 13–16 In general, these ciency and anaemia. In contrast, repetitive exercise periods symptoms are transient and can be considered protective at a relatively low intensity may have protective eVects on for critical organ damage: its progressive nature causes the the gastrointestinal tract. There is strong evidence that athlete to reduce exercise intensity or duration. Sometimes physical activity reduces the risk of colon cancer by up to the symptoms may be so serious that they can limit exercise 50%. Less convincing evidence exists for cholelithiasis and performance severely1 12 16 and even participation in physi- constipation. Physical activity may reduce the risk of diver- ticulosis, gastrointestinal haemorrhage, and inflammatory Incidence rates during prolonged exercise vary mostly bowel disease although this cannot be substantiated firmly.
from 20% to 50%, depending on factors such as mode, Up to now, underlying mechanisms are poorly understood duration, and intensity of exercise, type of symptom, age, although decreased gastrointestinal blood flow, neuro- training status, sex, dietary intake, occurrence of gastro- immuno-endocrine alterations, increased gastrointestinal intestinal symptoms at rest, and method of investiga- motility, and mechanical bouncing during exercise are tion.12 13 15 In particular, exercise intensity seems to be an postulated. Future research on exercise associated digestive processes should give more insight into the relationship toms.12 13 16 The mechanisms by which exercise causes gastrointestinal symptoms are not well known. Decreased gastrointestinal blood flow, increased gastrointestinalmotility, increased mechanical bouncing, and altered neu-roendocrine modulation are postulated.11–13 All of these Introduction
mechanisms are associated with exercise intensity.13 17–20 The impact of exercise and physical activity on the gastro- While most gastrointestinal symptoms do not hamper intestinal tract is an area of emerging interest. During the the athlete’s health, gastrointestinal bleeding may be a seri- past two decades research was mainly directed towards the ous problem. Most often the type of bleeding is occult and hazards of strenuous exercise, especially gastrointestinal transient, although anecdotal case reports document acute symptoms.1–3 In recent years, however, interest has also massive upper and lower gastrointestinal bleeding.21 focussed on the potential benefits of physical activity on the Repeated gastrointestinal bleeding during training and gastrointestinal tract. Several studies indicate an inverse competition may contribute to iron deficiency and relationship between physical activity and risk of gastro- anaemia.22 Also, endotoxaemia, malabsorption, gastro- intestinal related diseases such as colon cancer,4–6 diverticu- intestinal tract inflammation, and hypersensitivity reac- lar disease,7 cholelithiasis,8 9 or constipation.10 While the tions have been postulated to occur.13 14 21 23 All of these prevalence of these diseases is relatively high and increases eVects, however, can mostly be prevented by appropriate with age, participation in physical activity is relatively low dietary (for example, suYcient fluid intake) and other pre- cautions (for example, avoidance of large amounts of aspi- This review summarises the current state of knowledge rin and non-steroidal anti-inflammatory drugs).12 22 on the hazards of exercise and the potential benefits of In addition to gastrointestinal symptoms, unfavourable physical activity. “Exercise” is considered as voluntary eVects of exercise on liver function11 and peptic ulcer activation of skeletal muscle leading to short term eVects disease24 have been reported. However, in well trained (for minutes or hours) while “physical activity” is endurance-type sportsmen the increase in liver size can be considered as repetitive exercise periods leading to long interpreted as a physiological adaptation to increased term eVects (for days, weeks, months, or years). We focus energy expenditure rather than an expression of liver dam- on the role of physical activity in the prevention of several age.25 Abnormal high serum levels of bilirubin, aspartate diseases of the gastrointestinal tract and the postulated aminotransferase, and alkaline phosphatase are seldom mechanisms by which physical activity influences the observed in blood, underlining the fact that prolonged gastrointestinal tract. These mechanisms will be discussed strenuous exercise does not lead to serious hepatic damage.
more extensively at the end of this review. As potential haz-ards of exercise have been the subject of several reviews (forexample, see Moses,11 Peters et al,12 and Brouns and Beck- Abbreviations used in this paper: RR, relative risk; CD, Crohn’s
ers13), they will be discussed only briefly.
Peters, vanBerge-Henegouwen, de Vries, et al Only under extreme exercise conditions, such as heat subjects. Furthermore, it cannot be ruled out that in some shock, may hepatic damage occur.25 In the elderly, long studies the level of physical activity was already reduced as term physical activity even may improve liver function.26 Epidemiological studies24 27 show that physically de- Two recent large prospective studies8 9 showed a relative manding occupations may enhance the risk of peptic ulcer risk (RR) of cholelithiasis of 0.63 in men and 0.69 in disease, independent of several other risk factors such as women when comparing the most active with the most social class.27 However, these studies were hampered by inactive subjects, whereas sedentary lifestyle (watching tel- some limitations and pitfalls which question their conclu- evision or sitting) resulted in an increased risk (RR sions. Recently,28 no relationship between a history of pep- 1.11–3.32). A clear dose-response relationship was ob- tic ulcer and leisure time physical activity was found.
served, independent of several potential risk factors, Physical activity may even contribute to healing of gastric strongly suggesting that (symptomatic) cholelithiasis can and duodenal ulcers by normalisation of the microcircula- be prevented by physical activity, even beyond its benefit The mechanisms by which physical activity may Benefits
influence the pathogenesis of gall stones are poorly under- The potential benefits of physical activity concern mainly stood but decreased biliary cholesterol secretion, and eVects on cancer risk, cholelithiasis, gastrointestinal haem- enhanced gall bladder and colonic motility, all known to be orrhage, inflammatory bowel disease, diverticular disease, important for gall stone formation at rest,33 are postulated.
Moreover, many factors which are related to an increasedrisk of cholesterol gall stone disease, such as glucose toler- ance, high serum levels of insulin, triglycerides, and various To date, the risk of oesophageal, bile duct, or gall bladder gall bladder regulatory hormones such as cholecystokinin, cancers have not been examined in relation to physical and low serum levels of high density lipoprotein choles- activity. Concerning stomach cancer, the data are contro- terol, are favourably altered by physical activity.33 35 36 versial: one study reported a reduced risk while two didnot.30 No relationship between physical activity and risk of pancreatic cancers has been found,30 31 whereas rectal can- The only study which examined gastrointestinal haemor- cer risk was unrelated to physical activity in the majority of rhage and physical activity was a prospective cohort study with three years of follow up in 8205 elderly subjects.37 In contrast, there is overwhelming evidence that physical Only severe gastrointestinal haemorrhage was investigated.
activity reduces the risk of colon cancer (for example, see Physical activity was measured by self reported frequency World Cancer Research Fund/American Institute for Can- of walking, gardening, or vigorous physical activity (result- cer Research,4 Oliveria and Christos,5 and Colditz and col- ing in sweating) three years before the study baseline. A leagues6). Despite diVerent methods of assessing the summary variable for the three activities was also amount and diVerent types of physical activity (at work or calculated. For those participants doing the activity at least during leisure time), there is consistent evidence that three times per week, RR was significantly lower for walk- physically active men and women are at a reduced risk of ing (0.6) and for the summary variable (0.7) in comparison colon cancer (up to 50% reduction in incidence).6 This with sedentary subjects, independent of several other risk eVect is independent of other risk factors such as diet and factors such as age, sex, mobility, body mass index, or body weight characteristics. The types of activity that may health status. The RR for gardening (0.8) and vigorous be of benefit in preventing colon cancer are largely physical activity (0.7) was not significantly lower. The unknown. Studies analysing dose-response relationships authors hypothesised that a relatively increased gastro- suggest that more intense activity may confer greater pro- intestinal blood flow in physically active subjects reduced tection against the risk of colon cancer than less intense the risk of gastrointestinal haemorrhage.37 One should keep in mind that the findings of this study were restricted to The primary postulated mechanism is that physical severe haemorrhage in elderly subjects and that no data are activity reduces intestinal transit time which would limit available for less severe forms of haemorrhage or for the time of contact between the colon mucosa and cancer promoting contents. Enhancing intestinal transit time mayindirectly aVect the risk of colon cancer by lowering secondary bile acid concentration or by increasing faecal A limited number of studies have investigated the preven- short chain fatty acids.32 33 Other mechanisms related to tive eVect of physical activity on Crohn’s disease (CD) or colon cancer risk, such as impaired immune function, spe- ulcerative colitis (UC). Sonnenberg38 was the first to show cific dietary intake (for example, large amounts of alcohol a beneficial eVect of physical activity by comparing or fat, low amounts of dietary fibre), or an increase in body incidence rates of inflammatory bowel disease among sev- mass index, insulin resistance, prostaglandin and triglycer- eral occupations in 12 014 individuals. Sedentary and ides levels, body iron stores, and/or free radical scavenging physically less demanding occupations were associated enzyme activity, can be altered favourably by physical with a higher risk of inflammatory bowel disease than physically demanding occupations. As in other occupa-tional cross sectional studies, this study may have been hampered by limitations, for instance, less demanding Several studies have been published on the relationship occupations may have attracted the chronically ill and pre- between physical activity and cholelithiasis. While early vious occupations were not recorded. Persson and studies yielded controversial results, most of the later stud- colleagues39 confirmed this association in a case control ies suggest a protective eVect of physical activity.8 9 34 Many study in patients with CD, but not with UC. They found of the earlier studies in particular are hampered by several RR values of 0.6 and 0.5 for weekly and daily exercise, methodological drawbacks: no control for potential risk respectively. Since then, inconsistent results have been factors other than age (for example, body weight or diet), obtained: one case control study40 showed a reduced risk, small sample sizes, limited methods for physical activity both for physically active CD and UC patients, while assessment, and low variability in physical activity among another study in CD patients did not.41 Postulated under- Benefits and hazards of physical activity on the gastrointestinal tract lying mechanisms were the stress reducing eVects of physi- Biological mechanisms
cal activity as well as changes in local neuro-immuno- As mentioned above, the mechanisms by which exercise and physical activity influence the gastrointestinal tract are While the preventive eVect of physical activity remains poorly understood although decreased gastrointestinal inconclusive, it has become clear that physical activity is blood flow, increase in gastrointestinal motility, increased not harmful for patients with inflammatory bowel disease,42 mechanical bouncing, and neuro-immuno-endocrine al- despite acute exercise related responses, such as increased terations are postulated.11–13 However, most of the de- serum malondialdehyde levels and activated neutrophils.43 scribed mechanisms have only been investigated after acute Nevertheless, physical activity should be promoted as bouts of exercise. Whether or not these mechanisms are these patients have muscle weakness and are at risk of predictive of the long term eVects of physical activity osteoporosis.44 This risk is especially high with glucocorti- coid medication, which causes muscle atrophy andweakness, osteoporosis, and osteopenia.42 In addition, physical activity may reduce disease activity and improve During exercise, blood will primarily be shunted to the skin physical health, general well being, perceived stress, and and exercising muscles at the expense of the gastro- intestinal tract. Rowell and colleagues17 found a 60–70%decrease in splanchnic blood flow in humans exercising at A possible role of physical activity in reducing the risk of maximal exercise intensity, splanchnic blood flow may be diverticular disease was suggested by observations of Manousos and colleagues45 who found that diverticular Ischaemic damage has been proposed as a causal mech- disease was more prevalent among subjects with sedentary anism of gastrointestinal bleeding during and after occupations than in more active occupations. Recently, exercise. Although gastrointestinal blood loss is transient, Aldoori and colleagues7 also observed an inverse relation- ship with physical activity in a prospective cohort of 47 678 tions after exercise have been found, indicative of local American men during four years of follow up. After adjust- mucosal damage with an inflammatory response.21 Tran- ment for several factors such as dietary fibre intake, overall sient post-exercise lesions from the stomach to the colon physical activity reduced the risk of symptomatic diverticu- have been observed in athletes and the histological picture lar disease (for highest versus lowest extremes, RR=0.63).
indicates ischaemic damage.3 14 Critical ischaemic levels may be reached under extreme exercise conditions when (RR=0.60) than for non-vigorous activity (RR=0.93, NS).
hyperthermia, hypohydration, hypoglycaemia, hypoxia, or Several specific activities reduced the risk of diverticular a combination of these factors are present.13 In addition, disease but only for the combination of jogging and changes in blood viscosity, erythrocyte deformability, and running was the inverse relationship statistically signifi- aggregability during exercise56 may further compromise cant. An increase in colonic motor activity via hormonal, local blood flow. Epithelial cells become deprived of meta- vascular, and mechanical aspects, leading to a reduction in bolic substrates leading to necrosis and mucosal bleeding.
colonic transit time, was postulated as an underlying In theory, critical ischaemic levels and accumulation of metabolic waste products may induce malabsorption,hypersecretion, and increased gastrointestinal permeability with endotoxaemia. Findings for the eVect of exercise on Several cross sectional studies have shown an inverse inde- absorption and acid secretion are inconsistent: both a pendent relationship between constipation and physical decrease or no change in absorption57 and acid secretion58 59 activity (for example, see Everhart and colleagues,10 Donald and colleagues,46 and Kinnunen47). Also, two case intestinal permeability and mild leakage of endotoxins into control studies48 49 showed that the defecation pattern of the portal circulation have only been found at higher runners was “better” (less firm stools, higher defecation frequency, higher stool weight) than in inactive controls, afinding which could not be confirmed by the study of GASTROINTESTINAL MOTILITY AND BILE SALT METABOLISM Data on the eVect of exercise and physical activity on Inconsistent results were observed in patients who gastrointestinal motility are scarce and mostly indirectly participated in a physical activity programme. Meshkin- obtained and limited to acute exercise.20 62 63 The direct pour and colleagues48 studied eight constipated patients eVect of exercise on gastrointestinal motility has been during four weeks of light physical activity (walking five hypothesised to explain gastrointestinal symptoms such as days a week for one hour a day). The distance walked each heartburn (gastro-oesophageal reflux), vomiting, gastro- day progressively increased from 2.9 to 5.2 km, but consti- intestinal cramps, urge to defecate, and diarrhoea.13 pation did not change. Both Karam and Nies51 and Gastric emptying of liquids and solids appears to be Resende and colleagues52 showed an improvement in unchanged or slightly accelerated at lower exercise intensi- defecation pattern and reduced laxative use after a combined physical activity/nutrition programme in elderly delayed.18 59 64 The long term eVects of gastric emptying are patients but the eVect of physical activity alone was not inconsistent: Carrio and colleagues65 found that basal gas- studied. In all of these studies physical activity was of rela- tric emptying was faster in runners than in controls while Rehrer et al found no diVerence.64 Thus the eVect of physical activity on constipation seems Up to now two studies have focused on the eVects of likely, but has not been proved. Underlying mechanisms exercise and physical activity on gall bladder motility. An are unclear but a favourable eVect on colonic motility, acute bout of aerobic exercise increased gall bladder ejec- decreased blood flow to the gut, biomechanical bouncing tion fraction slightly but insignificantly in a healthy of the gut during running, compression of the colon by non-obese female population.66 Also, the eVect of physical abdominal musculature, and increased fibre intake as a activity was insignificant. In 27 obese female subjects who result of increased energy expenditure have all been exercised (45 minute brisk walking five times per week) for 12 weeks, postprandial gall bladder ejection fraction Peters, vanBerge-Henegouwen, de Vries, et al increased significantly, but this increase, although larger, did not diVer from that in the control group.67 Orocaecal transit time was reported to be unchanged, delayed, or accelerated20 53 68 after exercise. Harris and col-leagues69 found that a high energy intake, which is probablycorrelated with intensive physical activity, was significantlycorrelated with fast orocaecal transit.
Studies of the eVect of physical activity on colonic tran- sit time have mostly been conducted in healthy subjects and their results are conflicting, probably due to method-ological problems: four studies found accelerated transittime after physical activity53 54 70 71 while three observed no overall eVect.72–74 Resende and colleagues52 observed no significant changes in gastrointestinal transit time in 12 immobile long stay patients after 12 weeks of individualsessions of massage and physical activity (five days a week, Putative relationship between the incidence of some gastrointestinal diseases/symptoms and amount of physical activity, ranging from bed rest to marathon running or triathlon. The relationship Research on the eVect of exercise and physical activity on of other gastrointestinal diseases (that is, diverticulosis, gastrointestinal bile salt metabolism is mainly limited to animal studies.
haemorrhage, inflammatory bowel disease, peptic ulcer disease) is notdepicted due to limited evidence. These studies showed that physical activity of moderateintensity increased bile acid excretion.75–77 Part of these symptoms are acute and transient and do not hamper the changes were due to hyperphagia.75 Research on the eVect athlete’s health, repeated gastrointestinal bleeding during of physical activity and exercise on secondary bile acid for- training and competition may occasionally lead to iron mation and absorption in humans is scarce. In obese deficiency and anaemia. However, these and other patients, a decrease in the secondary/primary bile acid ratio symptoms can often be prevented with appropriate has been observed after treatment with a subcaloric diet and graded physical activity.78 Sutherland and colleagues79 Physical activity, mostly performed at a relatively low found that total faecal bile acid concentration was intensity, may also have protective eVects on the gastro- significantly lower in male distance runners than in seden- intestinal tract. There is strong evidence that physical tary men, while bile acid secretion was not diVerent activity reduces the risk of colon cancer. Less convincing between groups. The lower faecal bile acid concentrations evidence is found for cholelithiasis and constipation. The were mainly due to the higher fibre intake and subse- putative relationship between the incidence of these quently higher stool weight in runners.
gastrointestinal diseases/symptoms and amount of physicalactivity is shown in fig 1. Physical activity may reduce the risk of diverticulosis, gastrointestinal haemorrhage, and The frequency of most gastrointestinal symptoms is almost inflammatory bowel disease, although up to now there has twice as high during running than during other endurance been little research to substantiate this. Physical activity sports such as cycling or swimming, where up and down does not interfere with the healing process in inflammatory movements are more limited.1 12 The mechanical vibration bowel disease and will probably not reduce the risk of rec- of the body is more than doubled in running compared with cycling.80 The way in which this bouncing of the gut Future research on exercise associated digestive pro- aVects gastrointestinal function is still unknown.12 53 cesses in health or disease should explore the mechanismsinvolved in the potential benefits and hazards of physical activity and exercise on the gastrointestinal tract.
Many hormones associated with gastrointestinal functionat rest (secretion, absorption, and motility) alter during exercise, in terms of plasma concentrations: cholecystoki- nin, vasoactive intestinal peptide, secretin, pancreatic Department of Medical Physiology and Sports Medicine, polypeptide, somatostatin, peptide histidine isoleucine, University Medical Centre Utrecht, Utrecht, The Netherlands peptide YY, gastrin, glucagon, motilin, catecholamines, endorphins, and prostaglandins.13 81 82 However, direct proof that these hormones alter gut function during exercise or induce exercise related gastrointestinal symp- Departments of Surgery and Gastroenterology, University Medical Centre Utrecht, Utrecht, The Netherlands With respect to immune function, the current opinion is Correspondence to: Dr H P F Peters, Department of Medical Physiology and that physical activity of moderate intensity may protect Sports Medicine, University Medical Centre Utrecht, PO Box 85060, 3508AB Utrecht, The Netherlands.
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Microsoft word - michael zemel.doc

Michael Zemel Professor of Nutrition and Medicine Director, The Nutrition Institute The University of Tennessee 1215 W. Cumberland Avenue – Room 229 Knoxville, TN 37996-1920 865-974-6238         Education and Experience: B.S. (Nutritional Sciences), University of Wisconsin, Madison, 1976; M.S. (Nutritional Sciences), University of Wisconsin, Madison, 1978; Ph.

Title Diagnostic tools for hierarchical (multilevel) linear modelsAuthor Adam Loy <>Maintainer Adam Loy <>Description A suite of diagnostic tools for hierarchical (multilevel) linear models. The package offersnot only leverage and traditional deletion diagnostics (Cook'sdistance, covratio, covtrace, and MDFFITS) but also providesconvenience functio

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