Regular swimming before the induction of ulcer ameliorates oxidative gastric damage in rats: The anxiolytic effect of exercise

Elif BAHADIR, Dilek ÖZBEYLİ, Gizem MARDİNOĞLU, Fatma TEMİZ, Merve SAĞANAK, Hamide ŞAHİN, Meral YÜKSEL, Feriha ERCAN, Berrak YEĞEN
217

Öz


Objectives: To investigate the impact of exercise on ulcerogenesis.
Materials and Methods: Gastric ulcer was induced in Wistar
albino rats that were either kept sedentary or had swimming
exercise for 6 weeks. Under anesthesia, ulcer was induced by
applying acetic acid on the stomach serosa, while control rats had
sham-operation. On 3rd or 10th days of ulcer induction, anxiety
levels were measured and rats were decapitated for measuring
serum cortisol level, while gastric tissue samples were obtained for
histopathologic analysis and for determination of malondialdehyde
(MDA), glutathione (GSH) levels, myeloperoxidase (MPO)
activity, luminol- and lucigenin-enhanced chemiluminescence
(CL) and nitric oxide (NO) levels.
Results: In sedentary 3-day-ulcer group, gastric MPO activities
were elevated with concomitant reductions in GSH content, while
these changes were reversed in 10-day ulcer group. In exercised
3-day-ulcer group, all parameters were significantly reversed.
Increased lucigenin-CL was suppressed, while NO levels were
elevated by exercise. Histological analysis revealed lower lesion
scores in exercised groups. Serum cortisol levels were not different
among ulcer groups, but anxiety was suppressed by swimming
exercise in 3-day-ulcer group.
Conclusion: Regular swimming exercise ameliorated acetic
acid-induced oxidative damage of stomach via inhibition of
neutrophil infiltration and through anti-stress effect of exercise.
Regular exercise may be considered in facilitating the healing of
gastric ulcers.
Keywords: Acetic acid, Gastric ulcer, Exercise, Myeloperoxidase,
Anxiety




DOI: http://dx.doi.org/10.5472/MMJoa.2903.01

Referanslar


Sonnenberg A, Everhart JE. The prevalence of self-reported

peptic ulcer in the United States. Am J Public Health

;86:200-5. doi: 10.2105/AJPH.86.2.200

Chuong JJ, Fisher RL, Chuong RL, Spiro HM. Duodenal

ulcer. Incidence, risk factors, and predictive value of plasma

pepsinogen. Dig Dis Sci 1986;31:1178-84. doi: 10.1007/

BF01296515

Cheng Y, Macera CA, Davis DR, Blair SN. Physical activity

and peptic ulcers. Does physical activity reduce the risk of

developing peptic ulcers? West J Med 2000;173:101-7. doi:

1136/bjsm.34.2.116

Katschinski BD, Logan RF, Edmond M, Langman MJ.

Physical activity at work and duodenal ulcer risk. Gut

;32:983-6. doi: 10.1136/gut.32.9.983

Tamzali Y, Marguet C, Priymenko N, Lyazrhi F. Prevalence of

gastric ulcer syndrome in high-level endurance horses. Equine

Vet J 2011;43:141-4. doi: 10.1111/j.2042-3306.2010.00129.x

Halvorsen FA, Lyng J, Ritland S. Gastrointestinal bleeding in

marathon runners. Scand J Gastroenterol 1986;21:493-7. doi:

3109/00365528609015168

Rosenstock S, Jorgensen T, Bonnevie O, Andersen L.

Risk factors for peptic ulcer disease: a population based

prospective cohort study comprising 2416 Danish adults. Gut

;52:186-93. doi:10.1136/gut.52.2.186

Liu W, Sheng H, Xu Y, Liu Y, Lu J, Ni X. Swimming

exercise ameliorates depression-like behavior in chronically

stressed rats: relevant to proinflammatory cytokines and IDO

activation. Behav Brain Res 2013;242:110-6. doi: 110-6.

doi:10.1016/j.bbr.2012.12.041

Jones MP. The role of psychosocial factors in peptic ulcer

disease: beyond Helicobacter pylori and NSAIDs. J Psychosom

Res 2006;60:407-12. doi: 10.1016/j.jpsychores.2005.08.009

Jones MP, Maganti K. Symptoms, gastric function, and

psychosocial factors in functional dyspepsia. J Clin

Gastroenterol 2004;38:866-72. doi: 10.1097/00004836-

-00006

Sciolino NR, Holmes PV. Exercise offers anxiolytic potential:

a role for stress and brain noradrenergic-galaninergic

mechanisms. Neurosci Biobehav Rev 2012;36:1965-84. doi:

1016/j.neubiorev.2012.06.005

Scully D, Kremer J, Meade MM, Graham R, Dudgeon K.

Physical exercise and psychological well being: a critical

review. Br J Sports Med 1998;32:111-20. doi: 10.1136/

bjsm.32.2.111

Radak Z, Chung HY, Goto S. Systemic adaptation to oxidative

challenge induced by regular exercise. Free Radic Biol Med

;44:153-9. doi :10.1016/j.freeradbiomed.2007.01.029

McMurray RG, AC Hackney. Endocrine responses to exercise

and training. In: Garrett W, DT Kirkendall, eds. Exercise and

Sport Science. Philadelphia:Lippincott, Williams & Wilkins,

:135-162.

Ji LL, Gomez-Cabrera MC, Vina J. Exercise and hormesis:

activation of cellular antioxidant signaling pathway. Ann N Y

Acad Sci 2006;1067:425-35. doi: 10.1196/annals.1354.061

Navarro A, Gomez C, Lopez-Cepero JM, Boveris A.

Beneficial effects of moderate exercise on mice aging:

survival, behavior, oxidative stress, and mitochondrial

electron transfer. Am J Physiol Regul Integr Comp Physiol

;286:R505-11. doi: 10.1152/ajpregu.00208.2003

Quintanilha AT. Effects of physical exercise and/or vitamin

E on tissue oxidative metabolism. Biochem Soc Trans

;12:403-4. doi: 10.1042/bst0120403

Cakir B, Kasimay O, Kolgazi M, Ersoy Y, Ercan F, Yegen BC.

Stress-induced multiple organ damage in rats is ameliorated

by the antioxidant and anxiolytic effects of regular exercise.

Cell Biochem Funct 2010;28:469-79. doi: 10.1002/cbf.1679

Beavers KM, Brinkley TE, Nicklas BJ. Effect of exercise

training on chronic inflammation. Clin Chim Acta

;411:785-93. doi: 10.1016/j.cca.2010.02.069

Santos RV, Viana VA, Boscolo RA, et al. Moderate exercise

training modulates cytokine profile and sleep in elderly people.

Cytokine 2012;60:731-5. doi: 10.1016/j.cyto.2012.07.028

Veiga EC, Antonio EL, Bocalini DS, et al. Prior exercise training

does not prevent acute cardiac alterations after myocardial

infarction in female rats. Clinics (Sao Paulo) 2011;66:889-

doi: 10.1590/S1807-59322011000500028

Okabe S, Roth JL, Pfeiffer CJ. A method for experimental,

penetrating gastric and duodenal ulcers in rats. Observations

on normal healing. Am J Dig Dis 1971;16:277-84. doi:

1007/BF02235252

Brown GR, Nemes C. The exploratory behaviour of rats in

the hole-board apparatus: is head-dipping a valid measure of

neophilia? Behav Processes 2008;78:442-8. doi: 10.1016/j.

beproc.2008.02.019

Beutler E, Villacorte D, Kuhl W, Guinto E, Srivastava S.

Nonenzymatic conversion of human hexosaminidase A. J

Lab Clin Med 1975;86:195-203. doi: 10.1038/258262a0

Bradley PP, Priebat DA, Christensen RD, Rothstein G.

Measurement of cutaneous inflammation: estimation of

neutrophil content with an enzyme marker. J Invest Dermatol

;78:206-9. doi: 10.1111/1523-1747.ep12506462

Kikuchi K, Nagano T, Hayakawa H, Hirata Y, Hirobe M.

Real time measurement of nitric oxide produced ex vivo by

luminol-H2O2 chemiluminescence method. J Biol Chem

;268:23106-10. doi: 10.1016/S0304-3940(97)00648-4

Kikuchi K, Nagano T, Hayakawa H, Hirata Y, Hirobe M.

Detection of nitric oxide production from a perfused organ

by a luminol-H2O2 system. Anal Chem 1993;65:1794-9. doi:

1021/ac00061a025

Ozveri ES, Bozkurt A, Haklar G, et al. Estrogens ameliorate

remote organ inflammation induced by burn injury in rats.

Inflamm Res 2001;50:585-91. doi: 10.1007/pl00000238

Alessio HM, Hagerman AE, Nagy S, et al. Exercise

improves biomarkers of health and stress in animals fed

ad libitum. Physiol Behav 2005;84:65-72. doi: 10.1016/j.

physbeh.2004.10.010

Peters HP, De Vries WR, Vanberge-Henegouwen GP, Akkermans

LM. Potential benefits and hazards of physical activity and

exercise on the gastrointestinal tract. Gut 2001;48:435-9. doi:

1136/gut.48.3.435

Aldoori WH, Giovannucci EL, Rimm EB, et al. Prospective

study of physical activity and the risk of symptomatic

diverticular disease in men. Gut 1995;36:276-82. doi:

1136/gut.36.2.276

Leitzmann MF, Rimm EB, Willett WC, et al. Recreational

physical activity and the risk of cholecystectomy in

women. N Engl J Med 1999;341:777-84. doi: 10.1056/

NEJM199909093411101

Peters HP, Zweers M, Backx FJ, et al. Gastrointestinal

symptoms during long-distance walking. Med Sci Sports

Exerc 1999;31:767-73. doi: 10.1097/00005768-199906000-

Cheng Y, Macera CA, Davis DR, Blair SN. Does physical

activity reduce the risk of developing peptic ulcers? Br J

Sports Med 2000;34:116-21. doi: 10.1136/bjsm.34.2.116

Shephard RJ, Shek PN. Associations between physical

activity and susceptibility to cancer: possible mechanisms.

Sports Med 1998;26:293-315. doi: 10.2165/00007256-

-00002

Nieman DC. Immune response to heavy exertion. J Appl Physiol

(1985). 1997;82:1385-94. doi: 10.4135/9781412994149.n129

Efremushkin GG, Titova ZA, Molchanov AV, Nedoseko

OV, Burgsdorf OE. [The effect of combined treatment using

bicycle exercise with a free choice of the load parameters

on the hemodynamics in peptic ulcer patients]. Ter Arkh

;70:13-6. doi: 10.17116/terarkh201688210-15

Kasimay O, Guzel E, Gemici A, et al. Colitis-induced

oxidative damage of the colon and skeletal muscle is

ameliorated by regular exercise in rats: the anxiolytic role

of exercise. Exp Physiol 2006;91:897-906. doi: 10.1113/

expphysiol.2006.034439

Conn VS. Anxiety outcomes after physical activity

interventions: meta-analysis findings. Nurs Res 2010;59:224-

doi: 10.1097/nnr.0b013e3181dbb2f8

Jindal A, Mahesh R, Kumar B. Anxiolytic-like effect of

linezolid in experimental mouse models of anxiety. Prog

Neuropsychopharmacol Biol Psychiatry 2013;40:47-53. doi:

1016/j.pnpbp.2012.09.006

Munck A, Guyre PM, Holbrook NJ. Physiological functions of

glucocorticoids in stress and their relation to pharmacological

actions. Endocr Rev 1984;5:25-44. doi: 10.1210/edrv-5-1-25

Filaretova LP, Filaretov AA, Makara GB. Corticosterone

increase inhibits stress-induced gastric erosions in rats. Am

J Physiol 1998;274(6 Pt 1):G1024-30. doi: 10.1016/s0928-

(98)81155-3

Perretti M, Mugridge KG, Wallace JL, Parente L. Reduction

of aspirin-induced gastric damage in rats by interleukin-1

beta: possible involvement of endogenous corticosteroids. J

Pharmacol Exp Ther 1992;261:1238-47. doi: 10.1007/978-

-011-2982-4_17

Hackney AC. Stress and the neuroendocrine system:

the role of exercise as a stressor and modifier of stress.

Expert Rev Endocrinol Metab 2006;1:783-92. doi:

1586/17446651.1.6.783

Garrett WE, Kirkendall DT. Exercise and Sport Science.

Philadelphia: Lippincott Williams & Wilkins, 2000:144.

Hill EE, Zack E, Battaglini C, Viru M, Viru A, Hackney

AC. Exercise and circulating cortisol levels: the intensity

threshold effect. J Endocrinol Invest 2008;31:587-91. doi:

1007/bf03345606

Pique JM, Whittle BJ, Esplugues JV. The vasodilator role of

endogenous nitric oxide in the rat gastric microcirculation.

Eur J Pharmacol 1989;174:293-6. doi: 10.1016/0014-

(89)90324-5

Kwiecien S, Ptak-Belowska A, Krzysiek-Maczka G, et al.

Asymmetric dimethylarginine, an endogenous inhibitor

of nitric oxide synthase, interacts with gastric oxidative

metabolism and enhances stress-induced gastric lesions. J

Physiol Pharmacol 2012;63:515-24.

Konturek SJ, Brzozowski T, Majka J, Pytko-Polonczyk J,

Stachura J. Inhibition of nitric oxide synthase delays healing

of chronic gastric ulcers. Eur J Pharmacol 1993;239:215-7.

doi:10.1016/0014-2999(93)90997-v

Peters HP, Wiersma WC, Akkermans LM, Bol E, et

al. Gastrointestinal mucosal integrity after prolonged

exercise with fluid supplementation. Med Sci Sports Exerc

;32:134-42. doi: 10.1097/00005768-200001000-00020

Jungersten L, Ambring A, Wall B, Wennmalm A. Both

physical fitness and acute exercise regulate nitric oxide

formation in healthy humans. J Appl Physiol (1985).

;82:760-4. doi: 10.1046/j.1365-2281.1999.00212.x

Suzuki H, Nishizawa T, Tsugawa H, Mogami S, Hibi T. Roles

of oxidative stress in stomach disorders. J Clin Biochem Nutr

;50:35-9. doi: 10.3164/jcbn.11-115sr

Tanaka H, Dinenno FA, Monahan KD, Clevenger CM,

DeSouza CA, Seals DR. Aging, habitual exercise, and

dynamic arterial compliance. Circulation 2000;102:1270-5.

doi:10.1161/01.cir.102.11.1270




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