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Zarife Nigar Özdemir; Gökhan Tazegül; Pınar Kuru; Şeyda Bilgin; Semih Tiber Menteşe; Can Erzık; Serap Sırvancı; Berrak C Yegen

doi:10.5472/MMJ.2013.03125.1

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Year 2014, Volume: 27 Issue: 1, 13 - 20, 30.09.2015

Zarife Nigar Özdemir Gökhan Tazegül Pınar Kuru Şeyda Bilgin Semih Tiber Menteşe Can Erzık Serap Sırvancı Berrak C Yegen

https://doi.org/10.5472/MMJ.2013.03125.1

Cited By: 4

Abstract

Objective: Previous studies have demonstrated a higher incidence of ulcerative colitis in non-smokers. We investigated the beneficial effects of nicotine treatment on colitis-induced anxiety and oxidative colonic damage on rats.Materials and Methods: Wistar Albino (250-300 g) rats (n=40) were randomly divided into 5 groups as saline-treated colitis group, nicotine pre-treated colitis group, nicotine post-treated colitis group, continuously nicotine-treated colitis group and control group. Groups received intraperitoneal injections of saline or nicotine (0.1 mg/kg/day) for 15 days prior to and for 3 days following the colitis induction. Malondialdehyde (MDA) and glutathione (GSH) levels, myeloperoxidase (MPO), superoxide dismutase (SOD) and catalase (CAT) activities, histological evaluation and DNA fragmentation were studied in colonic samples. Anxiety levels were evaluated with the hole-board test. Results were evaluated using ANOVA and Mann-Whitney-U tests. Results: The saline-treated colitis group had increased MPO and MDA levels, DNA fragmentation and histological damage scores when compared with the control group. In the nicotinetreated groups MPO and MDA levels and DNA fragmentation were reduced, with lower histologic damage scores. Reduced SOD, CAT and GSH levels were also increased in nicotine-treated groups. Conclusion: This study demonstrates antioxidant effects of nicotine treatment in the acetic acid-induced colitis model including an increased antioxidant capacity, reduced migration of neutrophils to the inflamed colon and a reduction of membrane damage.

Keywords

Ulcerative colitis, Anxiety, Myeloperoxidase, Superoxide dismutase, Glutathione, Catalase

References

1. Lakatos PL. Recent trends in the epidemiology of inflammatory bowel diseases: Up or down? World J Gastroenterol 2006;12:6102–8.
2. Maritz GS, Mutemwa M. Tobacco smoking: patterns, health consequences for adults, and the long-term health of the offspring. Glob J Health Sci 2012; 30;4:62-75.
3. Harries AD, Baird A, and Rhodes J. Non-smoking: A feature of ulcerative colitis. Br Med J (Clin Res Ed). 1982; 284(6317):706. doi: 10.1136/bmj.284.6317.706
4. Koutroubakis I, Manousos ON, Menuwissen SG, Pena AS. Environmental risk factors in inflammatory bowel disease. Hepatogastroenterology 1996; 43: 381–93.
5. Graff LA, Walker JR, Bernstein CN. It’s not just about the gut: managing depression and anxiety in inflammatory bowel disease. Prac Gastroenterol 2010;34:11–25.
6. GilbertDG, Robinson,JH, Chamberlin CL, Spielberger CD. Effects of smoking/nicotine on anxiety, heart rate, and lateralization of EEG during a stressful movie. Psychophysiology1989;26:311-20. doi: 10.1111/j.1469-8986.1989.tb01924.x
7. Guslandi M, Tittobello A. Outcome of ulcerative colitis after treatment with transdermal nicotine. Eur J Gastroenterol Hepatol 1998;10:513- 5. doi: 10.1097/00042737-199806000-00014
8. Sandborn W, Tremaine W, Leighton J, et al. Nicotine tartrate liquid enemas for mildly to moderately active left-sided ulcerative colitis unresponsive to first-line therapy: a pilot study. Aliment Pharmacol Ther 1997;11:663-71. doi: 10.1046/j.1365-2036.1997.00208.x
9. Sandborn WJ, Tremaine WJ, Offord KP, et al.Transdermal nicotine for mildly to moderately active ulcerative colitis. A randomized, double-blind, placebo-controlled trial. Ann Intern Med 1997;126; 364-71. doi: 10.7326/0003-4819-126-5-199703010-00004
10. Lauritsen K, Laursen LS, Bukhave K, Rask-Madsen J. Inflammatory intermediates in inflammatory bowel disease. Int J Colorectal Dis 1989;4:75–90.
11. Brown SJ, Mayer L. The immune response in inflammatory bowel disease. Am J Gastroenterol 2007;102:2058-69. doi: 10.1111/ j.1572- 0241.2007.01343.x
12. Papadakis KA, Targan SR. Role of cytokines in the pathogenesis of inflammatory bowel disease. Annu Rev Med 2000;51:289-98. doi: 10.1146/annurev.med.51.1.289
13. Saareks V, Riutta A, Mucha I, Alanko J, Vapaatalo H. Nicotine and cotinine modulate eicosanoid production in human leukocytes and platelet rich plasma. Eur J Pharmacol 1993; 248: 345–9. doi: dx.doi. org/10.1016/0926-6917(93)90012-F
14. Zijlstra FJ, Scrivastava ED, Rhodes M, et al. Effect of nicotine on rectal mucus and mucosal eicosanoids. Gut 1994; 35: 247–51. doi: 10.1136/gut.35.2.247
15. Zijlstra FJ, Vincent JE, Mol WM, Hoogsteden HC, van Hal PTW, Jongejan RC. Eicosanoid levels in broncho alveolar lavage fluid of young female smokers and non-smokers. Eur J Clin Invest 1992; 22: 301–6.
16. Van Dijk JP, Madretsma GS, Keuskamp ZJ, Zijlstra FJ. Nicotine inhibits cytokine synthesis by mouse colonic mucosa. Eur J Pharmacol 1995 ;278: 11-2. doi: 10.1016/0014-2999(95)00211-3
17. Geng Y, Savage SM, Johnson LJ, Seagrave J, Sopori ML. Effects of nicotine on the immune response. I. Chronic exposure to nicotine impairs antigen receptor-mediated signal transduction in lymphocytes. Toxicol Appl Pharmacol 1995;135:268-278. doi: 10.1006/taap.1995. 1233
18. Geng Y, Savage SM, Razani-Boroujerdi S, Sopori ML. Effects of nicotine on the immune response. II.Chronic nicotine treatment induces T cell anergy. J Immunol 1996; 156:2384-90.
19. MacPherson B, Pfeiffer C. Experimental production of diffuse colitis in rats. Digestion 1978;17:135–50. doi: 10.1159/000198104
20. Marco EM, Llorente R, Pe´rez-A´lvarez L, Moreno E, Guaza C, Viveros MP . The κ-opioid receptor is involved in the stimulating effect of nicotine on adrenocortical activity but not in nicotine induced anxiety. Behav Brain Res 2005;163: 212–8. doi: 10.1016/j. bbr.2005.05.005
21. File SE, Wardill AG. Validity of head-dipping as a measure of exploration in a modified hole-board. Psychopharmacologia 1975;44: 53–9. doi: 10.1007/BF00421184
22. Boissier JR, Simon P. La reaction d’exploration chez la souris. Th´erapie 1962;17: 1225–32.
23. Beuge JA, Aust SD. Microsomal lipid peroxidation. Methods Enzymol 1978;52:302–10. doi: 10.1016/S0076-6879(78)52032-6
24. Beutler E. Glutathione in red blood cell methabolism. In: Beutler E, editor. A manual of biochemical methods. New York: Grune & Stratton, 1975:112–4.
25. Bradley PP, Priebat DA, Christersen RD, Rothstein G. Measurement of cutaneous inflammation: Estimation of neutrophil content with an enzyme marker. J Invest Dermatol 1982;78:206–9. doi: 10.1111/1523- 1747.ep12506462
26. Mylroie AA, Collins H, Umbles C, Kyle J. Erythrocyte superoxide dismutase activity and other parameters of copper status in rats ingesting lead acetate. Toxicol Appl Pharmacol 1986;82: 512–20. doi: 10.1016/0041-008X(86)90286-3.
27. Aebi H. Catalase in vitro. In: Bergmeyer HU, editor. Methods of Enzymatic Analysis. 2nd edition. New York: Verlag Chemie Weinheim Academic Press, 1974: 121–6.
28. Burton K. A study of the conditions and mechanism of the diphenylamine reaction for the colorimetric estimation of deoxyribonucleic acid. Biochem J 1956;62:315-23.
29. Benowitz NL, Jacob P 3rd. Daily intake of nicotine during cigarette smoking. Clin Pharmacol Ther 1984;354:499-504. doi: 10.1038/ clpt.1984.67
30. Sanahan F. Pathogenesis of ulcerative colitis. Lancet 1993;342: 407– 11.doi: 10.1016/0140-6736(93)92818-E
31. Samuelsson S. Ulceros Colit och Proktit [Dissertation]. Uppsala, Sweden: Department of Social Medicine, University of Uppsala, 1976.
32. Pullan RD, Rhodes J, Ganesh S, et al. Transdermal nicotine for active ulcerative colitis. N Engl J Med 1994;24:811-5. doi: 10.1056/ NEJM199403243301202
33. Ingram JR, Routledge P, Rhodes J, et al. Nicotine enemas for treatment of ulcerative colitis: a study of the pharmacokinetics and adverse events associated with three doses of nicotine. Aliment Pharmacol Ther 2008; 20:859-65. doi: 10.1111/j.1365- 2036.2004.02199.x
34. Thomas GA, Rhodes J, Ingram JR. Mechanism of disease: nicotine- a review of its actions in the context of gastrointestinal disease. Nat Clin Pract Gastroenterol Hepatol 2005;2:536-44. doi: 10.1038/ ncpgasthep0316
35. Cosnes J. What is the link between the use of tobacco and IBD? Inflamm Bowel Dis 2008;14:S14–5. doi: 10.1097/00054725- 200810001-00007
36. McGilligan VE, Wallace JM, Heavey PM, Ridley DL, Rowland IR. Hypothesis about mechanisms through which nicotine might exert its effect on the interdependence of inflammation and gut barrier function in ulcerative colitis. Inflamm Bowel Dis 2007; 13: 108–15. doi: 10.1002/ibd.20020
37. Nikfar S, Ehteshami-Ashar S, Rahimi R, Abdollahi M.. Systematic review and metaanalysis of the efficacy and tolerability of nicotine preparations in active ulcerative colitis. Clin Ther 2010; 32: 2304–15. doi: 10.1016/j.clinthera.2011.01.004.
38. Aldhous MC, Drummond HE, Anderson N, et al. Smoking habit and load influence age at diagnosis and disease extent in ulcerative colitis. Am J Gastroenterol 2007; 102: 589–97. doi: 10.1111/ j.1572- 0241.2007.01065.x
39. Bastida G, Beltrán B. Ulcerative colitis in smokers, non-smokers and exsmokers. World J Gastroenterol 2011; 17: 2740–7. doi: 10.3748/ wjg.v17.i22.2740
40. Birrenbach T, Böcker U. Inflammatory bowel disease and smoking: a review of epidemiology, pathophysiology, and therapeutic implications. Inflamm Bowel Dis 2004;10:848-59. doi: 10.1097/ 00054725-200411000-00019
41. van der Heide F, Dijkstra A, Weersma RK, et al. Effects of active and passive smoking on disease course of Crohn’s disease and ulcerative colitis. Inflamm Bowel Dis 2009; 15: 1199–207. doi: 10.1002/ ibd.20884.
42. Carlson NG, Bacchi A, Rogers SW, Gahring LC. Nicotine blocks TNF-alpha mediated neuroprotection to NMDA by an alphabungarotoxin-sensitive pathway. J Neurobiol 1998, 35:29-36.
43. Metz CN, Tracey KJ. It takes nerve to dampen inflammation. Nat Immunol 2005; 6:756-7. doi: 10.1038/ni0805-756
44. McGilligan VE, Wallace JM, Heavey PM, Ridley DL, Rowland IR. The effect of nicotine in vitro on the integrity of tight junctions in Caco-2 cell monolayers. Food Chem Toxicol 2007; 45:1593-8. doi: 10.1016/j.fct.2007.02.021
45. de Jonge WJ, Ulloa L. The alpha7 nicotinic acetylcholine receptor as a pharmacological target for inflammation. Br J Pharmacol 2007;151:915-29. doi: 10.1038/sj.bjp.0707264
46. Kolgazi M, Uslu U, Yuksel M, Velioglu-Ogunc A, Ercan F, Alican I. The role of cholinergic anti-inflammatory pathway in acetic acidinduced colonic inflammation in the rat. Chem Biol Interact. 2013 5;205:72-80. doi: 10.1016/j.cbi.2013.06.009.
47. Babbs CF. Oxygen radicals in ulcerative colitis. Free Radic Biol Med1992;13, 169–81. doi: 10.1016/0891-5849(92)90079-V 48. Hanauer S. Inflammatory bowel disease. N Engl J Med 1996; 334: 841-8. doi: 10.1056/NEJM199603283341307
49. Aoshiba K, Nagai A, Konno K. Nicotine prevents a reduction in neutrophil filterability induced by cigarette smoke exposure. Am J Respir Crit Care Med 1994;150:1101-7. doi: 10.1164/ajrccm.150.4. 7921443
50. Ko JK, Cho CH. The diverse actions of nicotine and different extracted fractions from tobacco smoke against hapten-induced colitis in rats. Toxicol Sci.2005;87:285-95. doi: 10.1093/toxsci/ kfi238
51. Eliakim R, Karmeli F, Rachmilewitz D, Cohen P, Fich A. Effect of chronic nicotine administration on trinitrobenzene sulphonic acidinduced colitis. Eur J Gastroenterol Hepatol 1998;10:1013-9. doi: 10.1097/00042737-199812000-00006
52. Maunder RG. Evidence that stress contributes to inflammatory bowel disease: evaluation, synthesis, and future directions. Inflamm Bowel Dis 2005;11:600–8. doi: 10.1097/01.MIB.0000161919.42878.a0
53. Kasimay O, Güzel 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 Sep;91:897-906. doi: 10.1113/expphysiol.2006.034439
54. Gulpinar MA, Ozbeyli D, Arbak S, Yegen BC. Anti-inflammatory effect of acute stress on experimental colitis is mediated by cholecystokinin-B receptors. Life Sci 2004;75, 77–91. doi: 10.1016/j. lfs.2003.12.009
55. Collins SM. Stress and the gastrointestinal tract IV. Modulation of intestinal inflammation by stress: basic mechanisms and the clinical relevance. Am J Physiol Gastrointest Liver Physiol 2001;280, G315– G318.
56. Picciotto MR, Brunzell DH, Caldarone BJ. Effect of nicotine and nicotinic receptors on anxiety and depression. Neuroreport. 2002;13:1097-106. doi: 10.1097/00001756-200207020-00006

Sıçanlarda kolite bağlı hasarı nikotin antioksidatif aktivitesi ile hafifletir

Year 2014, Volume: 27 Issue: 1, 13 - 20, 30.09.2015

Zarife Nigar Özdemir Gökhan Tazegül Pınar Kuru Şeyda Bilgin Semih Tiber Menteşe Can Erzık Serap Sırvancı Berrak C Yegen

https://doi.org/10.5472/MMJ.2013.03125.1

Cited By: 4

Abstract

Amaç: Epidemiyolojik çalışmalar ülseratif kolitin sigara
kullanmayanlarda daha sık görüldüğünü bildirmektedir. Bu
çalışmada kolitle oluşan oksidan hasar ve anksiyete üzerine nikotin
ön tedavisinin ve/veya kolit sonrası tedavinin olası yararlı etkilerinin
araştırılması amaçlanmıştır.
Gereç ve Yöntem: Wistar Albino (250-300 g) sıçanlar (n=40),
serum fizyolojik (SF) verilen, ön-tedavili, tedavili ve ön-tedavi+
tedavili kolit grubu ve kontrol grubu olmak üzere beşe ayrıldı. Kolit
öncesi 15 gün ve kolit sonrasında 3 gün sıçanlara intraperitoneal SF
ya da nikotin (0,1 mg/kg/gün) uygulandı. Kolon örneklerinde oksidan
hasarı belirlemek için malondialdehid (MDA), miyeloperoksidaz
(MPO) aktivitesi, glutatyon (GSH), süperoksit dismutaz (SOD),
katalaz ve DNA fragmantasyonu ölçümleri ile histolojik skorlama
yapıldı. Delikli kutu testi ile anksiyete seviyeleri belirlendi. Sonuçlar
ANOVA ve Mann Whitney U testi ile analiz edildi.
Bulgular: Kolitte artan anksiyetenin nikotin ile değişmediği
gözlendi. SF verilen kolit grubunda kolon MPO ve MDA düzeyleri
ile DNA fragmantasyonunun ve hasar skorunun kontrol grubuna
kıyasla arttığı, nikotin verilen tüm kolit gruplarında ise bu hasar
göstergelerinin anlamlı şekilde düştüğü gözlendi. Histolojik doku
hasarı skorunun nikotin uygulanan kolit grubunda daha az olduğu
gözlendi. SOD, katalaz ve GSH düzeylerindeki azalmanın nikotin
tedavisiyle anlamlı şekilde arttığı gözlendi.
Sonuç: Çalışmada asetik asitle oluşturulan kolit modelinde,
nikotin tedavisinin doku antioksidan kapasitesini arttırarak,
inflamasyon sonucu nötrofil göçünü ve membran hasarını azaltarak
antioksidan etki oluşturduğu gösterildi.

Keywords

Ulseratif kolit, Anksiyete, Miyeloperoksidaz, Superoksit dismutaz, Glutatyon, Katalaz

References

1. Lakatos PL. Recent trends in the epidemiology of inflammatory bowel diseases: Up or down? World J Gastroenterol 2006;12:6102–8.
2. Maritz GS, Mutemwa M. Tobacco smoking: patterns, health consequences for adults, and the long-term health of the offspring. Glob J Health Sci 2012; 30;4:62-75.
3. Harries AD, Baird A, and Rhodes J. Non-smoking: A feature of ulcerative colitis. Br Med J (Clin Res Ed). 1982; 284(6317):706. doi: 10.1136/bmj.284.6317.706
4. Koutroubakis I, Manousos ON, Menuwissen SG, Pena AS. Environmental risk factors in inflammatory bowel disease. Hepatogastroenterology 1996; 43: 381–93.
5. Graff LA, Walker JR, Bernstein CN. It’s not just about the gut: managing depression and anxiety in inflammatory bowel disease. Prac Gastroenterol 2010;34:11–25.
6. GilbertDG, Robinson,JH, Chamberlin CL, Spielberger CD. Effects of smoking/nicotine on anxiety, heart rate, and lateralization of EEG during a stressful movie. Psychophysiology1989;26:311-20. doi: 10.1111/j.1469-8986.1989.tb01924.x
7. Guslandi M, Tittobello A. Outcome of ulcerative colitis after treatment with transdermal nicotine. Eur J Gastroenterol Hepatol 1998;10:513- 5. doi: 10.1097/00042737-199806000-00014
8. Sandborn W, Tremaine W, Leighton J, et al. Nicotine tartrate liquid enemas for mildly to moderately active left-sided ulcerative colitis unresponsive to first-line therapy: a pilot study. Aliment Pharmacol Ther 1997;11:663-71. doi: 10.1046/j.1365-2036.1997.00208.x
9. Sandborn WJ, Tremaine WJ, Offord KP, et al.Transdermal nicotine for mildly to moderately active ulcerative colitis. A randomized, double-blind, placebo-controlled trial. Ann Intern Med 1997;126; 364-71. doi: 10.7326/0003-4819-126-5-199703010-00004
10. Lauritsen K, Laursen LS, Bukhave K, Rask-Madsen J. Inflammatory intermediates in inflammatory bowel disease. Int J Colorectal Dis 1989;4:75–90.
11. Brown SJ, Mayer L. The immune response in inflammatory bowel disease. Am J Gastroenterol 2007;102:2058-69. doi: 10.1111/ j.1572- 0241.2007.01343.x
12. Papadakis KA, Targan SR. Role of cytokines in the pathogenesis of inflammatory bowel disease. Annu Rev Med 2000;51:289-98. doi: 10.1146/annurev.med.51.1.289
13. Saareks V, Riutta A, Mucha I, Alanko J, Vapaatalo H. Nicotine and cotinine modulate eicosanoid production in human leukocytes and platelet rich plasma. Eur J Pharmacol 1993; 248: 345–9. doi: dx.doi. org/10.1016/0926-6917(93)90012-F
14. Zijlstra FJ, Scrivastava ED, Rhodes M, et al. Effect of nicotine on rectal mucus and mucosal eicosanoids. Gut 1994; 35: 247–51. doi: 10.1136/gut.35.2.247
15. Zijlstra FJ, Vincent JE, Mol WM, Hoogsteden HC, van Hal PTW, Jongejan RC. Eicosanoid levels in broncho alveolar lavage fluid of young female smokers and non-smokers. Eur J Clin Invest 1992; 22: 301–6.
16. Van Dijk JP, Madretsma GS, Keuskamp ZJ, Zijlstra FJ. Nicotine inhibits cytokine synthesis by mouse colonic mucosa. Eur J Pharmacol 1995 ;278: 11-2. doi: 10.1016/0014-2999(95)00211-3
17. Geng Y, Savage SM, Johnson LJ, Seagrave J, Sopori ML. Effects of nicotine on the immune response. I. Chronic exposure to nicotine impairs antigen receptor-mediated signal transduction in lymphocytes. Toxicol Appl Pharmacol 1995;135:268-278. doi: 10.1006/taap.1995. 1233
18. Geng Y, Savage SM, Razani-Boroujerdi S, Sopori ML. Effects of nicotine on the immune response. II.Chronic nicotine treatment induces T cell anergy. J Immunol 1996; 156:2384-90.
19. MacPherson B, Pfeiffer C. Experimental production of diffuse colitis in rats. Digestion 1978;17:135–50. doi: 10.1159/000198104
20. Marco EM, Llorente R, Pe´rez-A´lvarez L, Moreno E, Guaza C, Viveros MP . The κ-opioid receptor is involved in the stimulating effect of nicotine on adrenocortical activity but not in nicotine induced anxiety. Behav Brain Res 2005;163: 212–8. doi: 10.1016/j. bbr.2005.05.005
21. File SE, Wardill AG. Validity of head-dipping as a measure of exploration in a modified hole-board. Psychopharmacologia 1975;44: 53–9. doi: 10.1007/BF00421184
22. Boissier JR, Simon P. La reaction d’exploration chez la souris. Th´erapie 1962;17: 1225–32.
23. Beuge JA, Aust SD. Microsomal lipid peroxidation. Methods Enzymol 1978;52:302–10. doi: 10.1016/S0076-6879(78)52032-6
24. Beutler E. Glutathione in red blood cell methabolism. In: Beutler E, editor. A manual of biochemical methods. New York: Grune & Stratton, 1975:112–4.
25. Bradley PP, Priebat DA, Christersen RD, Rothstein G. Measurement of cutaneous inflammation: Estimation of neutrophil content with an enzyme marker. J Invest Dermatol 1982;78:206–9. doi: 10.1111/1523- 1747.ep12506462
26. Mylroie AA, Collins H, Umbles C, Kyle J. Erythrocyte superoxide dismutase activity and other parameters of copper status in rats ingesting lead acetate. Toxicol Appl Pharmacol 1986;82: 512–20. doi: 10.1016/0041-008X(86)90286-3.
27. Aebi H. Catalase in vitro. In: Bergmeyer HU, editor. Methods of Enzymatic Analysis. 2nd edition. New York: Verlag Chemie Weinheim Academic Press, 1974: 121–6.
28. Burton K. A study of the conditions and mechanism of the diphenylamine reaction for the colorimetric estimation of deoxyribonucleic acid. Biochem J 1956;62:315-23.
29. Benowitz NL, Jacob P 3rd. Daily intake of nicotine during cigarette smoking. Clin Pharmacol Ther 1984;354:499-504. doi: 10.1038/ clpt.1984.67
30. Sanahan F. Pathogenesis of ulcerative colitis. Lancet 1993;342: 407– 11.doi: 10.1016/0140-6736(93)92818-E
31. Samuelsson S. Ulceros Colit och Proktit [Dissertation]. Uppsala, Sweden: Department of Social Medicine, University of Uppsala, 1976.
32. Pullan RD, Rhodes J, Ganesh S, et al. Transdermal nicotine for active ulcerative colitis. N Engl J Med 1994;24:811-5. doi: 10.1056/ NEJM199403243301202
33. Ingram JR, Routledge P, Rhodes J, et al. Nicotine enemas for treatment of ulcerative colitis: a study of the pharmacokinetics and adverse events associated with three doses of nicotine. Aliment Pharmacol Ther 2008; 20:859-65. doi: 10.1111/j.1365- 2036.2004.02199.x
34. Thomas GA, Rhodes J, Ingram JR. Mechanism of disease: nicotine- a review of its actions in the context of gastrointestinal disease. Nat Clin Pract Gastroenterol Hepatol 2005;2:536-44. doi: 10.1038/ ncpgasthep0316
35. Cosnes J. What is the link between the use of tobacco and IBD? Inflamm Bowel Dis 2008;14:S14–5. doi: 10.1097/00054725- 200810001-00007
36. McGilligan VE, Wallace JM, Heavey PM, Ridley DL, Rowland IR. Hypothesis about mechanisms through which nicotine might exert its effect on the interdependence of inflammation and gut barrier function in ulcerative colitis. Inflamm Bowel Dis 2007; 13: 108–15. doi: 10.1002/ibd.20020
37. Nikfar S, Ehteshami-Ashar S, Rahimi R, Abdollahi M.. Systematic review and metaanalysis of the efficacy and tolerability of nicotine preparations in active ulcerative colitis. Clin Ther 2010; 32: 2304–15. doi: 10.1016/j.clinthera.2011.01.004.
38. Aldhous MC, Drummond HE, Anderson N, et al. Smoking habit and load influence age at diagnosis and disease extent in ulcerative colitis. Am J Gastroenterol 2007; 102: 589–97. doi: 10.1111/ j.1572- 0241.2007.01065.x
39. Bastida G, Beltrán B. Ulcerative colitis in smokers, non-smokers and exsmokers. World J Gastroenterol 2011; 17: 2740–7. doi: 10.3748/ wjg.v17.i22.2740
40. Birrenbach T, Böcker U. Inflammatory bowel disease and smoking: a review of epidemiology, pathophysiology, and therapeutic implications. Inflamm Bowel Dis 2004;10:848-59. doi: 10.1097/ 00054725-200411000-00019
41. van der Heide F, Dijkstra A, Weersma RK, et al. Effects of active and passive smoking on disease course of Crohn’s disease and ulcerative colitis. Inflamm Bowel Dis 2009; 15: 1199–207. doi: 10.1002/ ibd.20884.
42. Carlson NG, Bacchi A, Rogers SW, Gahring LC. Nicotine blocks TNF-alpha mediated neuroprotection to NMDA by an alphabungarotoxin-sensitive pathway. J Neurobiol 1998, 35:29-36.
43. Metz CN, Tracey KJ. It takes nerve to dampen inflammation. Nat Immunol 2005; 6:756-7. doi: 10.1038/ni0805-756
44. McGilligan VE, Wallace JM, Heavey PM, Ridley DL, Rowland IR. The effect of nicotine in vitro on the integrity of tight junctions in Caco-2 cell monolayers. Food Chem Toxicol 2007; 45:1593-8. doi: 10.1016/j.fct.2007.02.021
45. de Jonge WJ, Ulloa L. The alpha7 nicotinic acetylcholine receptor as a pharmacological target for inflammation. Br J Pharmacol 2007;151:915-29. doi: 10.1038/sj.bjp.0707264
46. Kolgazi M, Uslu U, Yuksel M, Velioglu-Ogunc A, Ercan F, Alican I. The role of cholinergic anti-inflammatory pathway in acetic acidinduced colonic inflammation in the rat. Chem Biol Interact. 2013 5;205:72-80. doi: 10.1016/j.cbi.2013.06.009.
47. Babbs CF. Oxygen radicals in ulcerative colitis. Free Radic Biol Med1992;13, 169–81. doi: 10.1016/0891-5849(92)90079-V 48. Hanauer S. Inflammatory bowel disease. N Engl J Med 1996; 334: 841-8. doi: 10.1056/NEJM199603283341307
49. Aoshiba K, Nagai A, Konno K. Nicotine prevents a reduction in neutrophil filterability induced by cigarette smoke exposure. Am J Respir Crit Care Med 1994;150:1101-7. doi: 10.1164/ajrccm.150.4. 7921443
50. Ko JK, Cho CH. The diverse actions of nicotine and different extracted fractions from tobacco smoke against hapten-induced colitis in rats. Toxicol Sci.2005;87:285-95. doi: 10.1093/toxsci/ kfi238
51. Eliakim R, Karmeli F, Rachmilewitz D, Cohen P, Fich A. Effect of chronic nicotine administration on trinitrobenzene sulphonic acidinduced colitis. Eur J Gastroenterol Hepatol 1998;10:1013-9. doi: 10.1097/00042737-199812000-00006
52. Maunder RG. Evidence that stress contributes to inflammatory bowel disease: evaluation, synthesis, and future directions. Inflamm Bowel Dis 2005;11:600–8. doi: 10.1097/01.MIB.0000161919.42878.a0
53. Kasimay O, Güzel 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 Sep;91:897-906. doi: 10.1113/expphysiol.2006.034439
54. Gulpinar MA, Ozbeyli D, Arbak S, Yegen BC. Anti-inflammatory effect of acute stress on experimental colitis is mediated by cholecystokinin-B receptors. Life Sci 2004;75, 77–91. doi: 10.1016/j. lfs.2003.12.009
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There are 55 citations in total.

Details

Primary Language	en.
Journal Section	Articles
Authors	Zarife Nigar Özdemir This is me Gökhan Tazegül This is me Pınar Kuru This is me Şeyda Bilgin This is me Semih Tiber Menteşe This is me Can Erzık This is me Serap Sırvancı This is me Berrak C Yegen This is me
Publication Date	September 30, 2015
Published in Issue	Year 2014 Volume: 27 Issue: 1

Cite

APA	Özdemir, Z. N., Tazegül, G., Kuru, P., Bilgin, Ş., et al. (2015). -. Marmara Medical Journal, 27(1), 13-20. https://doi.org/10.5472/MMJ.2013.03125.1
AMA	Özdemir ZN, Tazegül G, Kuru P, Bilgin Ş, Menteşe ST, Erzık C, Sırvancı S, Yegen BC. -. Marmara Med J. September 2015;27(1):13-20. doi:10.5472/MMJ.2013.03125.1
Chicago	Özdemir, Zarife Nigar, Gökhan Tazegül, Pınar Kuru, Şeyda Bilgin, Semih Tiber Menteşe, Can Erzık, Serap Sırvancı, and Berrak C Yegen. “-”. Marmara Medical Journal 27, no. 1 (September 2015): 13-20. https://doi.org/10.5472/MMJ.2013.03125.1.
EndNote	Özdemir ZN, Tazegül G, Kuru P, Bilgin Ş, Menteşe ST, Erzık C, Sırvancı S, Yegen BC (September 1, 2015) -. Marmara Medical Journal 27 1 13–20.
IEEE	Z. N. Özdemir, G. Tazegül, P. Kuru, Ş. Bilgin, S. T. Menteşe, C. Erzık, S. Sırvancı, and B. C. Yegen, “-”, Marmara Med J, vol. 27, no. 1, pp. 13–20, 2015, doi: 10.5472/MMJ.2013.03125.1.
ISNAD	Özdemir, Zarife Nigar et al. “-”. Marmara Medical Journal 27/1 (September 2015), 13-20. https://doi.org/10.5472/MMJ.2013.03125.1.
JAMA	Özdemir ZN, Tazegül G, Kuru P, Bilgin Ş, Menteşe ST, Erzık C, Sırvancı S, Yegen BC. -. Marmara Med J. 2015;27:13–20.
MLA	Özdemir, Zarife Nigar et al. “-”. Marmara Medical Journal, vol. 27, no. 1, 2015, pp. 13-20, doi:10.5472/MMJ.2013.03125.1.
Vancouver	Özdemir ZN, Tazegül G, Kuru P, Bilgin Ş, Menteşe ST, Erzık C, Sırvancı S, Yegen BC. -. Marmara Med J. 2015;27(1):13-20.

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