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may1
en1Departments of 1 Physiology2 Histology and Embryology, School of Medicine, Marmara University, Istanbul, Turkiye
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(Received 12 May 2006;
accepted after revision 6 June 2006; first published online 8 June 2006)
Corresponding author B. Ç. Yeen: Marmara University, School of Medicine, Haydarpa
a, Istanbul 34668, Türkiye. Email: byegen{at}marmara.edu.tr
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Introduction |
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Ulcerative colitis (UC) is an idiopathic inflammatory bowel disease (IBD) with diffuse, recurrent inflammation of the colon and rectum, which is predominantly characterized by cycles of acute inflammation, ulceration and bleeding of the colonic mucosa (Sanahan, 1993). The aetiology of UC is not clearly understood, but inflammatory mediators, such as cytokines and eicosanoids, and excessive production of reactive oxygen species (ROS) by the inflamed mucosa have been proposed to contribute significantly to the development of tissue injury (Babbs, 1992). In contrast, there is a long history of observations suggesting that psychological stress contributes to the course of IBD (Maunder, 2005) and that chronic stress increases the severity of intestinal inflammation (Gulpinar et al. 2004). Considering the improvements in psychological outcomes (i.e. reduction of depression and anxiety, and improved mood states) reached by habitual exercise (Byrne & Byrne, 1993), a number of studies have investigated the preventive effect of physical activity on inflammatory bowel diseases. Sonnenberg (1990) has shown that sedentary and physically less demanding occupations were associated with a higher risk of inflammatory bowel disease than physically demanding occupations. In contrast, the results of a case control study comparing incidence rates of IBD showed a reduced risk for physically active patients with Crohn's disease (CD) or UC, while in another study active CD patients had a high risk (Klein et al. 1998; Sorensen et al. 1987). Suggested underlying mechanisms in the preventive effect were the stress reducing effects of physical activity and changes in local neuro-immuno-endocrine effects (Loudon et al. 1999).
Although there is a large amount of research examining the impact of exercise on the gastrointestinal tract, most of the clinical studies conducted in humans had methodological limitations, making it difficult to explore the mechanisms involved in the potential benefits or hazards of physical activity on the intestinal tissue. Regarding the presence of insufficient information on the effects of regular exercise on the pathogenesis of colitis, the primary purpose of the present study was to examine the potential anxiolytic and protective effects of exercise in the underlying mechanisms of oxidative colonic injury. Another purpose of the study was to examine the effect of colonic injury on skeletal muscle, which was preconditioned to oxidative injury during the exercise training.
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Methods |
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Adult Sprague–Dawley rats of both sexes (n = 18) weighing 250–300 g were housed individually in a light- and temperature-controlled room on a 12 h–12 h light–dark cycle, in which the temperature (22 ± 2°C) and relative humidity (65–70%) were kept constant. The animals were fed a standard pellet lab chow, and food was withdrawn overnight before induction of colitis, but access to water was allowed ad libitum. The animals were randomly divided into three groups as: control (non-trained non-colitis-induced; n = 6), non-runner colitis (n = 6) and runner colitis groups (n = 6). The experiments were approved by the Marmara University School of Medicine Animal Care and Use Committee.
Training protocol
A rotarod (Northel, 
stanbul, Turkiye) with a 7 cm diameter rod and a constant acceleration capability (1 cm s–2) was used. The rod was elevated 40 cm above the floor of the cage. Before daily training, rats were allowed to accommodate on the rod for 5 min. Runner rats were subjected to low-intensity (7 m min–1; 30 min day–1; 3 days week–1) training for 6 weeks (Mitchell et al. 2004). During the running session, if the rat fell off the rod, a sensor was activated to stop rotation. Then the rat was put back on the rod until 30 min running time was completed. After the first week of training, rats were accustomed to run without any falls. Non-runner rats remained in their cages in the experiment room during the running period and were handled for an equal amount of time.
Induction of experimental colitis
At the end of 6 weeks and 1 h after the last exercise session, induction of colitis was performed. Before the induction of colitis, the rats were deprived of food, but not water, for 18 h. Colitis was induced by a modification of the method of MacPherson & Pfeiffer (1978). The induction of colitis was performed by intracolonic administration of 1 ml of 4% (v/v) acetic acid diluted in saline (pH 2.3) through a polyethylene tube (PE-60), the tip of which was positioned in the colon 8 cm past the anus under light ether anaesthesia. Acetic acid was slowly administered into the colonic lumen using ether inhalation. After a 30 s period of exposure, excess fluid was withdrawn, and the colon was then flushed with 1.5 ml of phosphate-buffered saline (pH 7.4). Control animals were subjected to the same procedure with the exception that isotonic saline was substituted for acetic acid.
Evaluation of anxiety
It is well known that an increase in anxiety reduces exploratory behaviour in rats, which can be tested by using the holeboard test (Marco et al. 2005). The holeboard apparatus, providing a measure of directed exploration in rats (File & Wardill, 1975), consisted of a wooden board (40 x 40 cm) with 16 equally spaced holes (each 13 cm in diameter).
The holeboard test was performed by placing the rat in the centre of the wooden board, and the test was recorded by a video camera for 5 min. Then the ‘freezing time’, when no movement of the trunk, head or extremities was observed was counted from the videotape (Boissier & Simon, 1962). Increased freezing time (as a percentage over 5 min) indicated a reduction in the exploratory behaviour and increased anxiety.
The holeboard test was first performed in both the runner and non-runner rats on the last day of the 6 week period before the induction of colitis. The test was repeated during the forty-eighth hour following acetic acid instillation.
Assessment of tissue injury
Macroscopic scoring. The rats were decapitated 72 h after the colonic instillation of saline or acetic acid, and the distal 8 cm of colons were opened down their mesenteric borders and cleansed of luminal contents. The severity of gross macroscopic damage in the colon was then graded using the following criteria modified from Wallace et al. (1992): 0, normal appearance; 1, focal hyperaemia, no ulcers; 2, single site of ulceration without associated inflammation; 3, single site of ulceration with inflammation 4, two or more sites of discrete ulceration and inflammation; 5, major site of injury or inflammation extending 1–2 cm along length of colon; and 6–10, score increased by one for each additional centimeter of damage or injury beyond 2 cm.
Biochemical measurements. Colon and gluteus muscle obtained from each animal were stored at –80°C until the determination of tissue myeloperoxidase (MPO) activity, lipid peroxidation (LP) and glutathione (GSH) levels. Tissue MPO activity is frequently utilized to estimate tissue neutrophil accumulation in inflamed tissues and has previously been shown to correlate significantly with the number of neutrophils determined histochemically in colonic tissues (Bradley et al. 1982). The method of assay of MPO activity in the present study was similiar to that previously described by others (Bradley et al. 1982). The tissue samples (0.2–0.3 g) were homogenized in 10 volumes of ice-cold potassium phosphate buffer (50 mM K2HPO4, pH 6.0) containing hexadecyltrimethylammonium bromide (HETAB; 0.5%, w/v). The homogenate was centrifuged at 41 400 g for 10 min at 4°C, and the supernatant was discarded. The pellet was then rehomogenized with an equivalent volume of 50 mM K2HPO4 containing 0.5% (w/v) HETAB and 10 mM EDTA (Sigma). Myeloperoxidase activity was assessed by measuring the H2O2-dependent oxidation of o-dianizidine.2HCl. One unit of enzyme activity was defined as the amount of MPO present per gram of tissue weight that caused a change in absorbance of 1.0 min–1 at 460 nm and 37°C.
Samples of colonic and muscle tissue were homogenized in 10 volumes of ice-cold 10% trichloracetic acid in an Ultra Turrax tissue homogenizer. Homogenized tissue samples were centrifuged at 2000 g for 15 min at 4°C. The supernatant was removed and recentrifuged at 41 400 g for 8 min. Gluthatione measurements were performed using a modification of the Ellman procedure (Aykaç et al. 1985). Lipid peroxidation was quantified by measuring the formation of thiobarbituric acid-reactive substances as previously described (Casini et al. 1986). Lipid peroxide levels were expressed in terms of malondialdehyde (MDA) equivalents using an extinction coefficient of 1.56 x 105 M–1 cm–1.
Histological analysis. For light microscopic investigations, samples from distal colon and gluteus muscle were fixed in 10% buffered p-formaldehyde and prepared for routine paraffin embedding. Sections of tissue were cut at 5 µm on a rotary microtome, mounted on slides, stained with Haematoxylin and Eosin (H&E), and examined under an Olympus BH 2 photomicroscope. All tissue sections were examined microscopically for characterization of histopathological changes by an experienced histologist (F.E.) who was unaware of the treatment conditions. Assessment of the colonic injury was performed using the previously described criteria: damage/necrosis (0, none; 1, localized; 2, moderate; 3, severe); submucosal oedema (0, none; 1, mild; 2, moderate; 3, severe); inflammatory cell infiltration (0, none; 1, mild; 2, moderate; 3, severe); vasculitis (0, none; 1, mild; 2, moderate; 3, severe); and perforation (0, absent; 1, present), with a maximum score of 13 (Gue et al. 1997). The histological analysis of the skeletal muscle was made using the criteria: disorganization of the muscle fibres (0, none; 1, mild; 2, moderate; 3, severe); and inflammatory cell infiltration (0, none; 1, mild; 2, moderate; 3, severe), with a maximum score of 6 (Erkanli et al. 2005).
Statistical analysis
The results are expressed as means ± S.E.M. with six rats per group. Instat statistical package (GraphPad Software, San Diego, CA, USA) was used. Following the assurance of normal distribution of data, one-way analysis of variance (ANOVA) was used for multiple comparisons and unpaired Student's t test was used to evaluate the level of statistical significance between two groups. Differences were considered statistically significant if P < 0.05.
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The occurrence of gastrointestinal symptoms, such as heartburn, nausea, vomiting, abdominal cramps, diarrhoea and gastrointestinal bleeding, is common during vigorous sports, causing the athlete to limit exercise performance by reducing exercise intensity or duration (Rehrer et al. 1989; Brouns & Beckers, 1993; Peters et al. 2001; Moses, 2005). Although the mechanisms by which exercise causes gastrointestinal symptoms are not well known, reduced gastrointestinal blood flow, increased gastrointestinal motility and mechanical bouncing, and alterations in neuroendocrine modulation have been suggested to play roles. In contrast, several studies indicate an inverse relationship between physical activity and the risk of gastrointestinal-related diseases, such as colonic cancer, cholelithiasis, diverticular disease or constipation (Peters et al. 2001). The primary postulated mechanisms include reduced intestinal transit time and enhanced activity of the free radical scavenging enzymes (Shephard & Shek, 1998). Accordingly, an inverse correlation was observed between the symptoms of irritable bowel syndrome and exercise (Colwell et al. 1998). However, inconsistent results have been obtained regarding the effect of physical activity on ulcerative colitis or Crohn's disease (Sorensen et al. 1987; Klein et al. 1998; Lee et al. 2005). The results of the present study demonstrate that regular running exercise in rats for 6 weeks reduces the severity of colitis-induced colonic damage by attenuating the oxidative tissue damage and enhancing the antioxidative enzyme activity.
It has been proposed that oxygen-derived free radicals are implicated in the pathogenesis of IBD (Simmonds et al. 1992; Simmonds & Rampton, 1993), while free radical-mediated lipid peroxidation is an important contributing factor in the development of acetic acid-mediated colonic damage (Xia et al. 1996). Several reports have shown that the formation of malondialdehyde, an end product of lipid peroxidation, is increased in the colonic tissue with inflammation (Yoshida et al. 1999; Mahgoub et al. 2003; Iseri et al. 2005). In accordance with the previous results, in the present study, acetic acid-induced colitis resulted in increased production of MDA in the colon. In contrast, regular exercise prior to colitis induction suppressed colonic MDA production, suggesting that exercise-induced preconditioning reduces lipid peroxidation and thereby supports the maintenance of cellular integrity. Interestingly, MDA production in the skeletal muscle was also elevated following colitis induction. Since acetic acid-induced colitis initiates a systemic inflammatory response, it appears that preconditioning through repetitive exercise provides protection not only for the colon but also for the remote targets of the inflammatory challenge.
Exercise is one of the physiological conditions characterized by increased production of free radicals (Clarkson, 1995). The production of free radicals increases in parallel with the increase in oxygen consumption during exercise, and this increase is directly related to the intensity and/or the duration of exercise (Ji, 1996). In contrast, the antioxidant enzymes, which constitute a defense mechanism against free radicals produced during exercise, are also affected by the exercise (Clarkson, 1995). Although much contradiction exists, it is generally accepted that regular physical activity leads to an increase in the activities of antioxidant enzymes, especially in muscles (Ji, 1993, 1996; Lawler & Powers, 1998). As well as the changes in exercising muscle, it was recently shown that exercise preconditioning inhibits inflammatory brain damage and decreases the expression of inflammatory mediators (Ding et al. 2005). It was reported that the protective effect of exercise might be due in part to suppression of the inflammatory process through reduced plasma levels of chemokines (Troseid et al. 2004).
One of the major constituents of intracellular protective mechanisms is glutathione, which provides protection against various noxious stimuli, including oxidative stress. Glutathione, as the main component of the endogenous non-protein sulfhydryl pool, is capable of repairing membrane lipid peroxides by interacting with free radicals to yield more stable elements (Ross, 1988; Shaw et al. 1990). Reduced GSH is known to be a major low molecular weight scavenger of free radicals in the cytoplasm (Shaw et al. 1990), limiting the propagation of free-radical reactions. Our results support the fact that depletion of colonic GSH is one of the major factors permitting lipid peroxidation and subsequent colonic damage. Since increased physical activity for 6 weeks prevented colonic GSH depletion, it appears that exercise supports the maintenance of antioxidant capacity in protecting the colonic tissue against oxidative stress. In accordance with the alterations in colonic GSH stores, colitis led to reduction in the GSH content of the skeletal muscle, supporting the generalized effect of colonic inflammation on the antioxidative status of the other tissues. Increased physical activity, in contrast, preserved the GSH content to protect the skeletal muscle against the systemic inflammatory response. In accordance with the present findings, Gunduz et al. (2004) have shown that long-term regular exercise increases the antioxidant capacity in rats. Furthermore, regular exercise attenuated lymphocyte apoptosis induced by oxidative stress, possibly by improving intracellular antioxidative capacity (Wang & Huang, 2005). In obese Zucker rats, exercise reversed the decreased enzyme activities of hepatic superoxide dismutase (SOD), GSH and glutathione peroxidase (Chang et al. 2004). Similarly, exercise training reduced oxidative stress via mechanisms that increased SOD activity in spontaneously hypertensive rats (Kohno et al. 2002).
It has been previously reported that active lesions in ulcerative colitis involve the migration of activated neutrophils and macrophages (Shiratora et al. 1989; Simmonds & Rampton, 1993). The tissue-associated MPO, which is known to provide an index of neutrophil infiltration, plays a fundamental role in oxidant production by neutrophils (Weiss & Ward, 1982). Exercise promotes the release of neutrophils into the circulation, and neutrophil activation during exercise may challenge endogenous antioxidant defence mechanisms (Peake & Suzuki, 2004). Our observations of elevated MPO levels in colonic tissues indicate that neutrophil accumulation contributes to the colitis-induced oxidative injury and that exercise appears to have a preventive effect through the inhibition of neutrophil infiltration. Exercise training in patients with claudication was shown to decrease neutrophil activation and degranulation and thereby reduce the inflammation (Turton et al. 2002). In principle, improved responsiveness of neutrophils to exercise of moderate intensity could mean that individuals participating in exercise may have improved resistance to infection (Peake, 2002). Conversely, competitive athletes undertaking regular intense exercise may be at greater risk of infections. In addition to exercise-induced reduction in colonic neutrophil accumulation, a similar suppression of neutrophils was evident in the muscle tissue accustomed to regular exercise.
Exercise-induced increases in aerobic fitness were shown to have beneficial short-term and long-term effects on psychological outcomes (DiLorenzo et al. 1999). Among the possible explanations for psychological outcomes are the direct effects of neurotransmitters (e.g. serotonin) in the brain that function to elevate mood (McDonald & Hodgdon, 1991; LaFontaine et al. 1992). The present data demonstrate that regular exercise attenuates the anxiety of the animals stressed when placed on the holeboards. However, in accordance with previous studies demonstrating that psychological stress might amplify intestinal inflammation (Collins, 2001), the severity of the colitis was enhanced as the level of anxiety was exaggerated. In contrast, the degree of anxiety was reduced in regularly exercised rats with significant attenuation of colonic inflammation. Similarly, physical activity was postulated to reduce disease activity and perceived stress in IBD patients, while general well-being and quality of life were improved (Loudon et al. 1999). Future research needs to examine the psychological benefits of exercise on colitis pathogenesis in non-clinical and clinical settings, to explain the correlation between the severity of colonic inflammation and the exercise intensity and duration.
In conclusion, this study implicates the importance of exercise as a non-pharmacological intervention in controlling the course of inflammatory bowel diseases, specifically during stressful conditions that trigger the exacerbation of the symptoms.
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P < 0.05 compared to non-colitis non-runner group.
