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Stress Management Affects Outcomes in the Pathophysiology of an Endometriosis Model

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Abstract

We have previously shown detrimental effects of stress in an animal model of endometriosis. We now investigated whether the ability to control stress can affect disease parameters. Endometriosis was surgically induced in female Sprague-Dawley rats before exposing animals to a controllable (submerged platform) or uncontrollable (no platform) swim stress protocol. Corticosterone levels and fecal pellet numbers were measured as an indicator of stress. Uncontrollable stress increased the number and size of the endometriotic cysts. Rats receiving uncontrollable stress had higher anxiety than those exposed to controllable stress or no stress and higher corticosterone levels. Uncontrollable stressed rats had more colonic damage and uterine cell infiltration compared to no stress, while controllable stress rats showed less of an effect. Uncontrollable stress also increased both colonic and uterine motility. In summary, the level of stress controllability appears to modulate the behavior and pathophysiology of endometriosis and offers evidence for evaluating therapeutic interventions.

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References

  1. Bulun SE, Utsunomiya H, Lin Z, et al. Steroidogenic factor 1 and endometriosis. Mol Cellular Endocrinol. 2009;300(1–2):104–108.

    Article  CAS  Google Scholar 

  2. Corson SL. Endometriosis: The Enigmatic Disease. EMIS-Canada, London, 1992.

    Google Scholar 

  3. Barnack JL, Chrisler JC. The experience of chronic illness in women: a comparison between women with chronic migraine headaches. Women Health. 2007;46(1);115–133.

    Article  PubMed  Google Scholar 

  4. Sepulcri Rde P, do Amaral VF. Depressive symptoms, anxiety, and quality of life in women with pelvic endometriosis. Eur J Obstet Gynecol Reprod Biol. 2009;142(1):53–56.

    Article  PubMed  Google Scholar 

  5. Low WY, Edelmann RJ, Sutton C. A psychological profile of endometriosis patients in comparison to patients with pelvic pain of other origins. J Psychosom Res. 1993;37(2):111–116.

    Article  CAS  PubMed  Google Scholar 

  6. Martin CE, Johnson E, Wechter ME, Leserman J, Zolnoun DA. Catastrophizing: a predictor of persistent pain among women with endometriosis at 1 year. Hum Reprod. 2011;26(11):3078–3084.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Petrelluzzi KF, Garcia MC, Petta CA, Grassi-Kassisse DM, Spadari-Bratfisch RC. Salivary Cortisol concentrations, stress and quality of life in women with endometriosis and chronic pelvic pain. Stress. 2008;11(5):390–397.

    Article  CAS  PubMed  Google Scholar 

  8. Vincent K, Warnaby C, Stagg CJ, Kennedy S, Tracey I. Dysmenorrhea is associated with ventral changes in otherwise healthy women. Pain. 2011;152(9):1966–1975.

    Article  PubMed  Google Scholar 

  9. Cuevas M, Flores I, Thompson KJ, Ramos-Ortolaza DL, Torres-Reveron A, Appleyard CB. Stress exacerbates endometriosis manifestations and inflammatory parameters in an animal model. Reprod Sci. 2012;19(8):851–862.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Konturek PC, Brzozowski T, Konturek SJ. Stress and the gut: pathophysiology, clinical consequences, diagnostic approach and treatment options. J Physiol Pharmacol. 2011;62(6):591–599.

    CAS  PubMed  Google Scholar 

  11. Rivat C, Becker C, Blugeot A, et al. Chronic stress induces transient spinal neuroinflammation, triggering sensory hypersensitivity and long-lasting anxiety-induced hyperalgesia. Pain. 2010; 150(2):358–368.

    Article  PubMed  Google Scholar 

  12. Tsigos C, Chrousos GP. Hypothalamic-pituitary-adrenal axis, neuroendocrine factors and stress. J Psychosom Res. 2002;53(4):865–871.

    Article  PubMed  Google Scholar 

  13. Friggi Sebe Petrelluzzi K, Garcia MC, Petta CA, et al. Physical therapy and psychological intervention normalize Cortisol levels and improve vitality in women with endometriosis. J Psychosom Obstet Gynaecol. 2012;33(4):191–198.

    Article  PubMed  Google Scholar 

  14. Vernon MW, Wilson EA. Studies on the surgical induction of endometriosis in the rat. Fertil Steril. 1985;44(5):684–694.

    Article  CAS  PubMed  Google Scholar 

  15. Appleyard CB, Cruz ML, Rivera E, Hernandez GA, Flores I. Experimental endometriosis in the rat is correlated with colonic motor function alterations but not with bacterial load. Reprod Sci. 2007;14(8):815–824.

    Article  PubMed  Google Scholar 

  16. Engelmann M, Ebner K, Landgraf R, Wotjak CT. Effects of Morris water maze testing on the neuroendocrine stress response and intrahypothalamic release of vasopressin and oxytocin in the rat. Horm Behavior. 2006;50(3):496–501.

    Article  CAS  Google Scholar 

  17. Maillot C, Million M, Wei JY, Gauthier A, Taché Y. Peripheral corticotropin-releasing factor and stress-stimulated colonic motor activity involve type 1 receptor in rats. Gastroenterology. 2000;119(6):1569–1579.

    Article  CAS  PubMed  Google Scholar 

  18. Walsh RN, Cummins RA. The open-field test: a critical review. Psychol Bull. 1976;83(3):482–504.

    Article  CAS  PubMed  Google Scholar 

  19. Ingelmo MR, Quereda F, Acién P. Intraperitoneal and subcutaneous treatment of experimental endometriosis with recombinant human interferon-α-2b in a murine model. Fertil Steril. 1999;71(5):907–911.

    Article  CAS  PubMed  Google Scholar 

  20. Hernández GA, Appleyard CB. Bacterial load in animal models of acute and chronic “reactivated” colitis. Digestion. 2003;67(3):161–169.

    Article  PubMed  Google Scholar 

  21. Boughton-Smith NK, Wallace JL, Whittle BJ. Relationship between arachidonic acid metabolism, myeloperoxidase activity and leukocyte infiltration in a rat model of inflammatory bowel disease. Agents Actions. 1998;25(1–2):115–123.

    Google Scholar 

  22. Bradley PP, Priebat DA, Christensen RD, Rothstein G. Measurement of cutaneous inflammation: estimation of neutrophil content with an enzyme marker. J Invest Derm. 1982;78(3):206–209.

    Article  CAS  PubMed  Google Scholar 

  23. Venkova K, Johnson AC, Myers B, Greenwood-Van Meerveld B. Exposure of the amygdala to elevated levels of corticosterone alters colonic motility in response to acute psychological stress. Neuropharmacology. 2010;58(7):1161–1167.

    Article  CAS  PubMed  Google Scholar 

  24. Bradesi S, Schwetz I, Ennes HS, et al. Repeated exposure to water avoidance stress in rats: a new model for sustained visceral hyperalgesia. Am J Physiol Gastrointest Liver Physiol. 2005;289(1):G42–G53.

    Article  CAS  PubMed  Google Scholar 

  25. Taché Y, Kiank C, Stengel A. A role for corticotropin-releasing factor in functional gastrointestinal disorders. Curr Gastroenterol Rep. 2009;11(4):270–277.

    Article  PubMed  Google Scholar 

  26. Cruz ML, Rodriguez VA, Altieri JS, et al. Effect of stress on the expression of nerve growth factor (NGF) and its receptor Trk-A in an animal model of endometriosis. FASEB J. 2011;25 (Meeting Abstract Supplement):849.2.

  27. Simon P, Dupuis R, Costentin J. Thigmotaxis as an index of anxiety in mice. Influence of dopaminergic transmissions. Behav Brain Res. 1994;61(1):59–64.

    Article  CAS  PubMed  Google Scholar 

  28. Larouche M, Kiank C, Tache Y. Corticotropin releasing factor signaling in colon and ileum: regulation by stress and pathophysiological implications. J Physiol Pharmacol. 2009;60(suppl 7): 33–46.

    Google Scholar 

  29. Larauche M, Gourcerol G, Million M, Adelson DW, Tache Y. Repeated psychological stress-induced alterations of visceral sensitivity and colonic motor functions in mice: influence of surgery and postoperative single housing on visceromotor responses. Stress. 2010;13(4):343–354.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Larauche M, Gourcerol G, Wang L, et al. Cortagine, a CRF1 agonist, induces stress like alterations of colonic function and visceral hypersensitivity in rodents primarily through peripheral pathways. Am J Physiol Gastrointest Liver Physiol. 2009;297(1):G215–G227.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Chen J Winston JH, Sarna SK. Neurological and cellular regulation of visceral hypersensitivity induced by chronic stress and colonic inflammation in rats. Neuroscience. 2013;248C:469–478.

    Article  CAS  Google Scholar 

  32. Sampson JA. Metastatic or embolic endometriosis, due to the menstrual dissemination of endometrial tissue into the venous circulation. Am J Pathol. 1927;3(2):93–110.

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Aguilar HN, Mitchell BF. Physiological pathways and molecular mechanisms regulating uterine contractility. Hum Reprod Update. 2010;16(6):725–744.

    Article  CAS  PubMed  Google Scholar 

  34. Forman A, Ulmsten U, Andersson KE. Aspects of inhibition of myometrial hyperactivity in primary dysmenorrhea. Acta Obstet Gynecol Scand Suppl. 1983;113:71–76.

    Article  CAS  PubMed  Google Scholar 

  35. Chen Y, Zhu B, Zhang H, Liu X, Guo SW. Epigallocatechin-3-gallate reduces myometrial infiltration, uterine hyperactivity, and stress levels and alleviates generalized hyperalgesia in mice induced with adenomyosis. Reprod Sci. 2013;20(12):1478–1491.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  36. Cryan JF, Markou A, Lucki I. Assessing antidepressant activity in rodents: recent developments and future needs. Trends Pharmacol Sci. 2002;23(5):238–245.

    Article  CAS  PubMed  Google Scholar 

  37. Christiansen JP, Greenwood BN. Stress-protective neural circuits: not all roads lead through the prefrontal cortex. Stress. 2013;17(1):1–12.

    Article  PubMed  Google Scholar 

  38. Kavushansky A, Vouimba RM, Cohen H, Richter-Levin G. Activity and plasticity in the CAI, the dentate gyrus, and the amygdale following controllable vs. uncontrollable water stress. Hippocampus. 2006;16(1):35–42.

    Article  PubMed  Google Scholar 

  39. Eriksen HL, Gunnersen KF, Sørensen JA, Munk T, Nielsen T, Knudsen UB. Psychological aspects of endometriosis: differences between patients with or without pain on four psychological variables. Eur J Obstet Gynecol Reprod Biol. 2008;139(1):100–105.

    Article  PubMed  Google Scholar 

  40. Müller MJ. Depressive attribution style and stressor uncontrollability increase perceived pain intensity after electric skin stimuli in healthy young men. Pain Res Manag. 2013;18(4):203–206.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Quartana PJ, Campbell CM, Edwards RR. Pain catastrophizing: a critical review. Expert Rev Neurother. 2009;9(5):745–758.

    Article  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Physiology and Pharmacology, Ponce School of Medicine and Health Sciences, 395 Zona Ind Reparada 2, 00716-2347, Ponce, PR, USA

    Caroline B. Appleyard PhD, Myrella L. Cruz MT, Siomara Hernández BS & Kenira J. Thompson PhD

  2. Public Health Program, Ponce School of Medicine and Health Sciences, Ponce, PR, USA

    Manuel Bayona MD, PhD

  3. Department of Microbiology, Ponce School of Medicine and Health Sciences, Ponce, PR, USA

    Idhaliz Flores PhD

Authors
  1. Caroline B. Appleyard PhD
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  2. Myrella L. Cruz MT
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  3. Siomara Hernández BS
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  4. Kenira J. Thompson PhD
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  5. Manuel Bayona MD, PhD
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  6. Idhaliz Flores PhD
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Corresponding author

Correspondence to Caroline B. Appleyard PhD.

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Appleyard, C.B., Cruz, M.L., Hernández, S. et al. Stress Management Affects Outcomes in the Pathophysiology of an Endometriosis Model. Reprod. Sci. 22, 431–441 (2015). https://doi.org/10.1177/1933719114542022

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  • DOI: https://doi.org/10.1177/1933719114542022

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