Research Article
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Year 2022, Volume: 39 Issue: 4, 1169 - 1174, 29.10.2022

Abstract

References

  • 1. Monnikes H, Tebbe JJ, Hildebrandt M, Arck P, Osmanoglou E, Rose M, et al. Role of stress in functional gastrointestinal disorders - Evidence for stress-induced alterations in gastrointestinal motility and sensitivity. Digest Dis. 2001;19(3):201-11.
  • 2. Duan C, Chen C, Ouyang Z, Duan C, Zhang S, Shang H, et al. Association of stress and functional gastrointestinal disorders in high school graduates. J Affect Disord. 2021;292:305-10.
  • 3. Richter JE. Stress and psychologic and environmental factors in functional dyspepsia. Scand J Gastroenterol Suppl. 1991;182:40-6.
  • 4. Bonilla S, Saps M. Early life events predispose the onset of childhood functional gastrointestinal disorders. Rev Gastroenterol Mex. 2013;78(2):82-91.
  • 5. Winston JH, Sarna SK. Enhanced sympathetic nerve activity induced by neonatal colon inflammation induces gastric hypersensitivity and anxiety-like behavior in adult rats. Am J Physiol Gastrointest Liver Physiol. 2016;311(1):G32-9.
  • 6. Enck P, Azpiroz F, Boeckxstaens G, Elsenbruch S, Feinle-Bisset C, Holtmann G, et al. Functional dyspepsia. Nat Rev Dis Primers. 2017;3:17081.
  • 7. Talley NJ, Goodsall T, Potter M. Functional dyspepsia. Aust Prescr. 2017;40(6):209-13.
  • 8. Asano H, Tomita T, Nakamura K, Yamasaki T, Okugawa T, Kondo T, et al. Prevalence of Gastric Motility Disorders in Patients with Functional Dyspepsia. J Neurogastroenterol Motil. 2017;23(3):392-9.
  • 9. Tack J, Piessevaux H, Coulie B, Caenepeel P, Janssens J. Role of impaired gastric accommodation to a meal in functional dyspepsia. Gastroenterology. 1998;115(6):1346-52.
  • 10. Zhang AZ, Wang QC, Huang KM, Huang JG, Zhou CH, Sun FQ, et al. Prevalence of depression and anxiety in patients with chronic digestive system diseases: A multicenter epidemiological study. World journal of gastroenterology. 2016;22(42):9437-44.
  • 11. Ye Y, Wang XR, Zheng Y, Yang JW, Yang NN, Shi GX, et al. Choosing an Animal Model for the Study of Functional Dyspepsia. Can J Gastroenterol Hepatol. 2018;2018:1531958.
  • 12. Liu LS, Winston JH, Shenoy MM, Song GQ, Chen JD, Pasricha PJ. A rat model of chronic gastric sensorimotor dysfunction resulting from transient neonatal gastric irritation. Gastroenterology. 2008;134(7):2070-9.
  • 13. Li S, Chen JD. Down-regulation of A-type potassium channel in gastric-specific DRG neurons in a rat model of functional dyspepsia. Neurogastroenterol Motil. 2014;26(7):962-70.
  • 14. Abdel-Aziz H, Wadie W, Zaki HF, Muller J, Kelber O, Efferth T, et al. Novel sequential stress model for functional dyspepsia: Efficacy of the herbal preparation STW5. Phytomedicine : international journal of phytotherapy and phytopharmacology. 2015;22(5):588-95.
  • 15. Jing FC, Zhang J, Feng C, Nian YY, Wang JH, Hu H, et al. Potential rat model of anxiety-like gastric hypersensitivity induced by sequential stress. World journal of gastroenterology. 2017;23(42):7594-608.
  • 16. Tominaga K, Fujikawa Y, Tanaka F, Kamata N, Yamagami H, Tanigawa T, et al. Structural changes in gastric glial cells and delayed gastric emptying as responses to early life stress and acute adulthood stress in rats. Life Sci. 2016;148:254-9.
  • 17. Winston JH, Aguirre JE, Shi XZ, Sarna SK. Impaired Interoception in a Preclinical Model of Functional Dyspepsia. Dig Dis Sci. 2017;62(9):2327-37.
  • 18. Sinen O, Bulbul M. The role of autonomic pathways in peripheral apelin-induced gastrointestinal dysmotility: involvement of the circumventricular organs. Exp Physiol. 2021;106(2):475-85.
  • 19. Sinen O, Ozkan A, Agar A, Bulbul M. Neuropeptide-S prevents 6-OHDA-induced gastric dysmotility in rats. Brain Res. 2021;1762:147442.
  • 20. Myers B, Greenwood-Van Meerveld B. Divergent effects of amygdala glucocorticoid and mineralocorticoid receptors in the regulation of visceral and somatic pain. Am J Physiol Gastrointest Liver Physiol. 2010;298(2):G295-303.
  • 21. Schrader AJ, Taylor RM, Lowery-Gionta EG, Moore NLT. Repeated elevated plus maze trials as a measure for tracking within-subjects behavioral performance in rats (Rattus norvegicus). Plos One. 2018;13(11).
  • 22. Galeano P, Martino Adami PV, Do Carmo S, Blanco E, Rotondaro C, Capani F, et al. Longitudinal analysis of the behavioral phenotype in a novel transgenic rat model of early stages of Alzheimer's disease. Front Behav Neurosci. 2014;8:321.
  • 23. Choung RS, Talley NJ. Novel mechanisms in functional dyspepsia. World journal of gastroenterology. 2006;12(5):673-7.
  • 24. Kindt S, Tack J. Impaired gastric accommodation and its role in dyspepsia. Gut. 2006;55(12):1685-91.
  • 25. Tang L, Zeng Y, Li L, Wang J, Peng D, Zhang T, et al. Electroacupuncture Upregulated Ghrelin in Rats with Functional Dyspepsia via AMPK/TSC2/Rheb-Mediated mTOR Inhibition. Dig Dis Sci. 2020;65(6):1689-99.
  • 26. Ji E, Wang T, Guo F, Zhang Y, Tang C, Tang D, et al. Xiaoerfupi alleviates the symptoms of functional dyspepsia by regulating the HTR3A and c-FOS. Biomed Pharmacother. 2019;120:109442.
  • 27. Babygirija R, Bulbul M, Yoshimoto S, Ludwig K, Takahashi T. Central and peripheral release of oxytocin following chronic homotypic stress in rats. Auton Neurosci. 2012;167(1-2):56-60.
  • 28. Yoshimoto S, Cerjak D, Babygirija R, Bulbul M, Ludwig K, Takahashi T. Hypothalamic circuit regulating colonic transit following chronic stress in rats. Stress. 2012;15(2):227-36.
  • 29. Jing F, Zhang J. Metabolic kinetics of 5-hydroxytryptamine and the research targets of functional gastrointestinal disorders. Dig Dis Sci. 2014;59(11):2642-8.
  • 30. Carola V, D'Olimpio F, Brunamonti E, Mangia F, Renzi P. Evaluation of the elevated plus-maze and open-field tests for the assessment of anxiety-related behaviour in inbred mice. Behav Brain Res. 2002;134(1-2):49-57.
  • 31. Otsuka T, Nishii A, Amemiya S, Kubota N, Nishijima T, Kita I. Effects of acute treadmill running at different intensities on activities of serotonin and corticotropin-releasing factor neurons, and anxiety- and depressive-like behaviors in rats. Behavioural Brain Research. 2016;298:44-51.
  • 32. Bolukbas I, Mundorf A, Freund N. Maternal separation in rats induces neurobiological and behavioral changes on the maternal side. Sci Rep. 2020;10(1):22431.
  • 33. Daniels WM, Pietersen CY, Carstens ME, Stein DJ. Maternal separation in rats leads to anxiety-like behavior and a blunted ACTH response and altered neurotransmitter levels in response to a subsequent stressor. Metab Brain Dis. 2004;19(1-2):3-14.
  • 34. Frye CA, Walf AA. Changes in progesterone metabolites in the hippocampus can modulate open field and forced swim test behavior of proestrous rats. Horm Behav. 2002;41(3):306-15.
  • 35. Koss WA, Gehlert DR, Shekhar A. Different effects of subchronic doses of 17-beta estradiol in two ethologically based models of anxiety utilizing female rats. Horm Behav. 2004;46(2):158-64.
  • 36. Bowman RE, Ferguson D, Luine VN. Effects of chronic restraint stress and estradiol on open field activity, spatial memory, and monoaminergic neurotransmitters in ovariectomized rats. Neuroscience. 2002;113(2):401-10.

Sex-Related Differences in Anxiety in Experimental Functional Dyspepsia Induced by Chronic Stress

Year 2022, Volume: 39 Issue: 4, 1169 - 1174, 29.10.2022

Abstract

Functional dyspepsia (FD) is associated with gastric sensorimotor dysfunction (including delayed gastric emptying (GE)) and psychosocial comorbidities. Anxiety is among the many psychiatric disorders that are related to FD. The aim of this study was to compare the effectiveness of chronic sequential stress to create an experimental FD model in male and female rats. The FD model was established by neonatal maternal separation (MS) early in life and repeated homotypic stress (RHS) in adulthood. Newborn pups from postnatal day 1 to day-21 underwent MS for 3 h. In adulthood, the control or maternally separated rats were loaded with RHS for 7 days comprised of 90-min restraint stress. The anxiety-like behaviors were evaluated by the open field (OF) and elevated plus maze (EPM) tests. To validate the experimental FD model, body weight and solid GE were measured in rats after the behavioral experiments. Compared with control males, body weight and GE were significantly (p<0.05) decreased in stressed rats, but not in females. Exposed to chronic stress male rats appeared to exhibit more anxiety-like behavior than control male rats on the OF and EPM. In contrast to the males, no significant differences were found in female groups. Unlike female rats, the male rats appear to be highly suitable to create an experimental FD model under chronic sequential stressed conditions. Therefore, anxious behaviors may not be observed in females due to the absence of dyspeptic symptoms.

References

  • 1. Monnikes H, Tebbe JJ, Hildebrandt M, Arck P, Osmanoglou E, Rose M, et al. Role of stress in functional gastrointestinal disorders - Evidence for stress-induced alterations in gastrointestinal motility and sensitivity. Digest Dis. 2001;19(3):201-11.
  • 2. Duan C, Chen C, Ouyang Z, Duan C, Zhang S, Shang H, et al. Association of stress and functional gastrointestinal disorders in high school graduates. J Affect Disord. 2021;292:305-10.
  • 3. Richter JE. Stress and psychologic and environmental factors in functional dyspepsia. Scand J Gastroenterol Suppl. 1991;182:40-6.
  • 4. Bonilla S, Saps M. Early life events predispose the onset of childhood functional gastrointestinal disorders. Rev Gastroenterol Mex. 2013;78(2):82-91.
  • 5. Winston JH, Sarna SK. Enhanced sympathetic nerve activity induced by neonatal colon inflammation induces gastric hypersensitivity and anxiety-like behavior in adult rats. Am J Physiol Gastrointest Liver Physiol. 2016;311(1):G32-9.
  • 6. Enck P, Azpiroz F, Boeckxstaens G, Elsenbruch S, Feinle-Bisset C, Holtmann G, et al. Functional dyspepsia. Nat Rev Dis Primers. 2017;3:17081.
  • 7. Talley NJ, Goodsall T, Potter M. Functional dyspepsia. Aust Prescr. 2017;40(6):209-13.
  • 8. Asano H, Tomita T, Nakamura K, Yamasaki T, Okugawa T, Kondo T, et al. Prevalence of Gastric Motility Disorders in Patients with Functional Dyspepsia. J Neurogastroenterol Motil. 2017;23(3):392-9.
  • 9. Tack J, Piessevaux H, Coulie B, Caenepeel P, Janssens J. Role of impaired gastric accommodation to a meal in functional dyspepsia. Gastroenterology. 1998;115(6):1346-52.
  • 10. Zhang AZ, Wang QC, Huang KM, Huang JG, Zhou CH, Sun FQ, et al. Prevalence of depression and anxiety in patients with chronic digestive system diseases: A multicenter epidemiological study. World journal of gastroenterology. 2016;22(42):9437-44.
  • 11. Ye Y, Wang XR, Zheng Y, Yang JW, Yang NN, Shi GX, et al. Choosing an Animal Model for the Study of Functional Dyspepsia. Can J Gastroenterol Hepatol. 2018;2018:1531958.
  • 12. Liu LS, Winston JH, Shenoy MM, Song GQ, Chen JD, Pasricha PJ. A rat model of chronic gastric sensorimotor dysfunction resulting from transient neonatal gastric irritation. Gastroenterology. 2008;134(7):2070-9.
  • 13. Li S, Chen JD. Down-regulation of A-type potassium channel in gastric-specific DRG neurons in a rat model of functional dyspepsia. Neurogastroenterol Motil. 2014;26(7):962-70.
  • 14. Abdel-Aziz H, Wadie W, Zaki HF, Muller J, Kelber O, Efferth T, et al. Novel sequential stress model for functional dyspepsia: Efficacy of the herbal preparation STW5. Phytomedicine : international journal of phytotherapy and phytopharmacology. 2015;22(5):588-95.
  • 15. Jing FC, Zhang J, Feng C, Nian YY, Wang JH, Hu H, et al. Potential rat model of anxiety-like gastric hypersensitivity induced by sequential stress. World journal of gastroenterology. 2017;23(42):7594-608.
  • 16. Tominaga K, Fujikawa Y, Tanaka F, Kamata N, Yamagami H, Tanigawa T, et al. Structural changes in gastric glial cells and delayed gastric emptying as responses to early life stress and acute adulthood stress in rats. Life Sci. 2016;148:254-9.
  • 17. Winston JH, Aguirre JE, Shi XZ, Sarna SK. Impaired Interoception in a Preclinical Model of Functional Dyspepsia. Dig Dis Sci. 2017;62(9):2327-37.
  • 18. Sinen O, Bulbul M. The role of autonomic pathways in peripheral apelin-induced gastrointestinal dysmotility: involvement of the circumventricular organs. Exp Physiol. 2021;106(2):475-85.
  • 19. Sinen O, Ozkan A, Agar A, Bulbul M. Neuropeptide-S prevents 6-OHDA-induced gastric dysmotility in rats. Brain Res. 2021;1762:147442.
  • 20. Myers B, Greenwood-Van Meerveld B. Divergent effects of amygdala glucocorticoid and mineralocorticoid receptors in the regulation of visceral and somatic pain. Am J Physiol Gastrointest Liver Physiol. 2010;298(2):G295-303.
  • 21. Schrader AJ, Taylor RM, Lowery-Gionta EG, Moore NLT. Repeated elevated plus maze trials as a measure for tracking within-subjects behavioral performance in rats (Rattus norvegicus). Plos One. 2018;13(11).
  • 22. Galeano P, Martino Adami PV, Do Carmo S, Blanco E, Rotondaro C, Capani F, et al. Longitudinal analysis of the behavioral phenotype in a novel transgenic rat model of early stages of Alzheimer's disease. Front Behav Neurosci. 2014;8:321.
  • 23. Choung RS, Talley NJ. Novel mechanisms in functional dyspepsia. World journal of gastroenterology. 2006;12(5):673-7.
  • 24. Kindt S, Tack J. Impaired gastric accommodation and its role in dyspepsia. Gut. 2006;55(12):1685-91.
  • 25. Tang L, Zeng Y, Li L, Wang J, Peng D, Zhang T, et al. Electroacupuncture Upregulated Ghrelin in Rats with Functional Dyspepsia via AMPK/TSC2/Rheb-Mediated mTOR Inhibition. Dig Dis Sci. 2020;65(6):1689-99.
  • 26. Ji E, Wang T, Guo F, Zhang Y, Tang C, Tang D, et al. Xiaoerfupi alleviates the symptoms of functional dyspepsia by regulating the HTR3A and c-FOS. Biomed Pharmacother. 2019;120:109442.
  • 27. Babygirija R, Bulbul M, Yoshimoto S, Ludwig K, Takahashi T. Central and peripheral release of oxytocin following chronic homotypic stress in rats. Auton Neurosci. 2012;167(1-2):56-60.
  • 28. Yoshimoto S, Cerjak D, Babygirija R, Bulbul M, Ludwig K, Takahashi T. Hypothalamic circuit regulating colonic transit following chronic stress in rats. Stress. 2012;15(2):227-36.
  • 29. Jing F, Zhang J. Metabolic kinetics of 5-hydroxytryptamine and the research targets of functional gastrointestinal disorders. Dig Dis Sci. 2014;59(11):2642-8.
  • 30. Carola V, D'Olimpio F, Brunamonti E, Mangia F, Renzi P. Evaluation of the elevated plus-maze and open-field tests for the assessment of anxiety-related behaviour in inbred mice. Behav Brain Res. 2002;134(1-2):49-57.
  • 31. Otsuka T, Nishii A, Amemiya S, Kubota N, Nishijima T, Kita I. Effects of acute treadmill running at different intensities on activities of serotonin and corticotropin-releasing factor neurons, and anxiety- and depressive-like behaviors in rats. Behavioural Brain Research. 2016;298:44-51.
  • 32. Bolukbas I, Mundorf A, Freund N. Maternal separation in rats induces neurobiological and behavioral changes on the maternal side. Sci Rep. 2020;10(1):22431.
  • 33. Daniels WM, Pietersen CY, Carstens ME, Stein DJ. Maternal separation in rats leads to anxiety-like behavior and a blunted ACTH response and altered neurotransmitter levels in response to a subsequent stressor. Metab Brain Dis. 2004;19(1-2):3-14.
  • 34. Frye CA, Walf AA. Changes in progesterone metabolites in the hippocampus can modulate open field and forced swim test behavior of proestrous rats. Horm Behav. 2002;41(3):306-15.
  • 35. Koss WA, Gehlert DR, Shekhar A. Different effects of subchronic doses of 17-beta estradiol in two ethologically based models of anxiety utilizing female rats. Horm Behav. 2004;46(2):158-64.
  • 36. Bowman RE, Ferguson D, Luine VN. Effects of chronic restraint stress and estradiol on open field activity, spatial memory, and monoaminergic neurotransmitters in ovariectomized rats. Neuroscience. 2002;113(2):401-10.
There are 36 citations in total.

Details

Primary Language English
Subjects Health Care Administration
Journal Section Clinical Research
Authors

Osman Sinen 0000-0002-3554-5604

Publication Date October 29, 2022
Submission Date June 20, 2022
Acceptance Date July 4, 2022
Published in Issue Year 2022 Volume: 39 Issue: 4

Cite

APA Sinen, O. (2022). Sex-Related Differences in Anxiety in Experimental Functional Dyspepsia Induced by Chronic Stress. Journal of Experimental and Clinical Medicine, 39(4), 1169-1174.
AMA Sinen O. Sex-Related Differences in Anxiety in Experimental Functional Dyspepsia Induced by Chronic Stress. J. Exp. Clin. Med. October 2022;39(4):1169-1174.
Chicago Sinen, Osman. “Sex-Related Differences in Anxiety in Experimental Functional Dyspepsia Induced by Chronic Stress”. Journal of Experimental and Clinical Medicine 39, no. 4 (October 2022): 1169-74.
EndNote Sinen O (October 1, 2022) Sex-Related Differences in Anxiety in Experimental Functional Dyspepsia Induced by Chronic Stress. Journal of Experimental and Clinical Medicine 39 4 1169–1174.
IEEE O. Sinen, “Sex-Related Differences in Anxiety in Experimental Functional Dyspepsia Induced by Chronic Stress”, J. Exp. Clin. Med., vol. 39, no. 4, pp. 1169–1174, 2022.
ISNAD Sinen, Osman. “Sex-Related Differences in Anxiety in Experimental Functional Dyspepsia Induced by Chronic Stress”. Journal of Experimental and Clinical Medicine 39/4 (October 2022), 1169-1174.
JAMA Sinen O. Sex-Related Differences in Anxiety in Experimental Functional Dyspepsia Induced by Chronic Stress. J. Exp. Clin. Med. 2022;39:1169–1174.
MLA Sinen, Osman. “Sex-Related Differences in Anxiety in Experimental Functional Dyspepsia Induced by Chronic Stress”. Journal of Experimental and Clinical Medicine, vol. 39, no. 4, 2022, pp. 1169-74.
Vancouver Sinen O. Sex-Related Differences in Anxiety in Experimental Functional Dyspepsia Induced by Chronic Stress. J. Exp. Clin. Med. 2022;39(4):1169-74.