Abstract
Endometriosis is a gynecological condition affecting 10% of women in reproductive age. High rates of depression and anxiety are observed in these patients. The mechanisms underlying endometriosis-induced behavioral alterations are still elusive. Animal models provide a useful tool to study the temporal sequence and biological pathways involved in this disease and comorbid states. Here, we sought to characterize time-related behavioral alterations in rats submitted to endometriosis model (EM) induced by peritoneal auto-transplantation of uterine tissues weekly for three weeks. Corticosterone stress reactivity, oxidative stress markers – reduced glutathione (GSH), lipid peroxidation, activity of superoxide dismutase (SOD) and myeloperoxidase (MPO) - and brain-derived-neurotrophic factor (BDNF) levels in the hippocampus were also evaluated. We observed a progressive increase in anxiety-like behavior from 14th to 21st days post-EM. Despair-like behavior was observed from the 14th day post-EM on, while anhedonia and apathetic-like behaviors accompanied by increased corticosterone stress response were detected on 21 days post-EM. Increased pain sensitivity was observed from the 7th day post-EM and was accompanied by increased endometrioma weight. The pro-oxidative alterations, decreased GSH and increased SOD activity were observed on 21 days post-EM, except for lipid peroxidation that was altered from the 14th day. Decreased BDNF also occurred on the 21st day. Therefore, this study demonstrates that EM is related to several features of clinical depression and proposes the contribution of hippocampal oxidative state and neurotrophic support for the emergence of these changes. Our results support the use of this model as a useful tool to test new strategies for endometriosis-related neuropsychiatric symptoms.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Archer J (1973) Tests for emotionality in rats and mice: a review. Anim Behav 21:205–235
Arnhold J, Flemmig J (2010) Human myeloperoxidase in innate and acquired immunity. Arch Biochem Biophys 500:92–106. https://doi.org/10.1016/j.abb.2010.04.008
As-sanie S, Harris RE, Napadow V et al (2012) Changes in regional gray matter volume in women with chronic pelvic pain : a voxel-based morphometry study. Pain 153:1006–1014. https://doi.org/10.1016/j.pain.2012.01.032
As-Sanie S, Harris RE, Harte SE et al (2013) Increased pressure pain sensitivity in women with chronic pelvic pain. Obstet Gynecol 122:1047–1055. https://doi.org/10.1097/AOG.0b013e3182a7e1f5
As-Sanie S, Kim J, Schmidt-Wilcke T (2016) Functional connectivity is associated with altered brain chemistry in women with endometriosis-associated chronic pelvic pain. J Pain 17:1–13. https://doi.org/10.1016/j.jpain.2015.09.008
Aznaurova YB, Zhumataev MB, Roberts TK et al (2014) Molecular aspects of development and regulation of endometriosis. Reprod Biol Endocrinol 12:50. https://doi.org/10.1186/1477-7827-12-50
Baj G, D’Alessandro V, Musazzi L et al (2012) Physical exercise and antidepressants enhance BDNF targeting in hippocampal CA3 dendrites: further evidence of a spatial code for BDNF splice variants. Neuropsychopharmacology 37:1600–1611. https://doi.org/10.1038/npp.2012.5
Bannerman D, Rawlins JN, McHugh S et al (2004) Regional dissociations within the hippocampus—memory and anxiety. Neurosci Biobehav Rev 28:273–283. https://doi.org/10.1016/j.neubiorev.2004.03.004
Bannon AW, Malmberg AB (2007) Models of nociception: hot-plate, tail-Flick, and formalin tests in rodents. In: current protocols in neuroscience. John Wiley & Sons, Inc, Hoboken, pp 8.9.1–8.9.16
Beissner F, Preibisch C, Schweizer-Arau A et al (2016) Psychotherapy with somatosensory stimulation for endometriosis-associated pain: the role of the anterior Hippocampus. Biol Psychiatry 84:1–9. https://doi.org/10.1016/j.biopsych.2017.01.006
Bilici M, Efe H, Köroğlu MAA et al (2001) Antioxidative enzyme activities and lipid peroxidation in major depression: alterations by antidepressant treatments. J Affect Disord 64:43–51. https://doi.org/10.1016/S0165-0327(00)00199-3
Biswas SK (2016) Does the interdependence between oxidative stress and inflammation explain the antioxidant paradox? Oxidative Med Cell Longev 2016:17–19. https://doi.org/10.1155/2016/5698931
Black CN, Bot M, Scheffer PG et al (2015) Is depression associated with increased oxidative stress? A systematic review and meta-analysis. Psychoneuroendocrinology 51:164–175. https://doi.org/10.1016/j.psyneuen.2014.09.025
Bouvier E, Brouillard F, Molet J et al (2017) Nrf2-dependent persistent oxidative stress results in stress-induced vulnerability to depression. Mol Psychiatry 22:1701–1713. https://doi.org/10.1038/mp.2016.144
Bruner-Tran KL, Mokshagundam S, Herington JL et al (2018) Rodent models of experimental endometriosis: identifying mechanisms of disease and therapeutic targets. Curr Women s Heal Rev 14:173–188. https://doi.org/10.2174/1573404813666170921162041
Budni J, Zomkowski AD, Engel D et al (2013) Folic acid prevents depressive-like behavior and hippocampal antioxidant imbalance induced by restraint stress in mice. Exp Neurol 240:112–121. https://doi.org/10.1016/j.expneurol.2012.10.024
Burke HM, Davis MC, Otte C, Mohr DC (2005) Depression and cortisol responses to psychological stress: a meta-analysis. Psychoneuroendocrinology 30:846–856. https://doi.org/10.1016/j.psyneuen.2005.02.010
Butte JC, Kakihana R, Noble EP (1978) The fluorometric assay of rat plasma corticosterone: evaluation of nonspecific fluorescence. Steroids 32:607–614
Carvalho ACF, Polineto OB, Crippa JADS et al (2015) Associations between chronic pelvic pain and psychiatric disorders and symptoms. Arch Clin Psychiatry (São Paulo) 42:25–30. https://doi.org/10.1590/0101-60830000000042
Chen L-C, Hsu J-W, Huang K-L et al (2016) Risk of developing major depression and anxiety disorders among women with endometriosis: a longitudinal follow-up study. J Affect Disord 190:282–285. https://doi.org/10.1016/j.jad.2015.10.030
Cox BM, Alsawah F, McNeill PC et al (2011) Neurochemical, hormonal, and behavioral effects of chronic unpredictable stress in the rat. Behav Brain Res 220:106–111. https://doi.org/10.1016/j.bbr.2011.01.038
Cuevas M, Flores I, Thompson KJ et al (2012) Stress exacerbates endometriosis manifestations and inflammatory parameters in an animal model. Reprod Sci 19:851–862. https://doi.org/10.1177/1933719112438443
Culley L, Law C, Hudson N et al (2017) The social and psychological impact of endometriosis on women's lives: a critical narrative review. Hum Reprod Update 19:625–639. https://doi.org/10.1093/humupd/dmt027
Cummings AM, Metcalf JL (1995) Induction of endometriosis in mice: a new model sensitive to estrogen. Reprod Toxicol 9:233–238
D’Souza D, Sadananda M (2017) Estrous cycle phase-dependent changes in anxiety- and depression-like profiles in the late adolescent Wistar-Kyoto rat. Ann Neurosci 24:136–145. https://doi.org/10.1159/000477151
de Lima CB, Cordeiro FB, Camargo M et al (2017) Follicular fluid lipid peroxidation levels in women with endometriosis during controlled ovarian hyperstimulation. Hum Fertil 20:48–54. https://doi.org/10.1080/14647273.2016.1246753
Dienes KA, Hazel NA, Hammen CL (2013) Cortisol secretion in depressed, and at-risk adults. Psychoneuroendocrinology 38:927–940. https://doi.org/10.1016/j.psyneuen.2012.09.019
Donnez J, Ph D, Binda M et al (2016) Oxidative stress in the pelvic cavity and its role in the pathogenesis of endometriosis. Fertil Steril 106:1–7. https://doi.org/10.1016/j.fertnstert.2016.07.1075
Gaweł S, Wardas M, Niedworok E, Wardas P (2004) Malondialdehyde (MDA) as a lipid peroxidation marker. Wiad Lek 57:453–455
Gupta S, Agarwal A, Krajcir N, Alvarez JG (2006) Article role of oxidative stress in endometriosis. Reprod BioMed Online 13:126–134. https://doi.org/10.1016/S1472-6483(10)62026-3
Gur A, Cevik R, Sarac AJ et al (2004) Hypothalamic-pituitary-gonadal axis and cortisol in young women with primary fibromyalgia: the potential roles of depression, fatigue, and sleep disturbance in the occurrence of hypocortisolism. Ann Rheum Dis 63:1504–1506. https://doi.org/10.1136/ard.2003.014969
Hannibal KE, Bishop MD (2014) Chronic stress, cortisol dysfunction, and pain: a psychoneuroendocrine rationale for stress management in pain rehabilitation. Phys Ther 94:1816–1825. https://doi.org/10.2522/ptj.20130597
Herken H, Gurel A, Selek S et al (2007) Adenosine deaminase, nitric oxide, superoxide dismutase, and xanthine oxidase in patients with major depression: impact of antidepressant treatment. Arch Med Res 38:247–252. https://doi.org/10.1016/j.arcmed.2006.10.005
Hernandez S, Cruz ML, Seguinot II et al (2017) Impact of psychological stress on pain perception in an animal model of endometriosis. Reprod Sci 24:1371–1381. https://doi.org/10.1177/1933719116687655
Huong NT, Matsumoto K, Kasai R et al (1998) In vitro antioxidant activity of Vietnamese ginseng saponin and its components. Biol Pharm Bull 21:978–981
Isingrini E, Camus V, Le Guisquet A-M et al (2010) Association between repeated unpredictable chronic mild stress (UCMS) procedures with a high fat diet: a model of fluoxetine resistance in mice. PLoS One 5:e10404. https://doi.org/10.1371/journal.pone.0010404
Janssen EB, Rijkers ACM, Hoppenbrouwers K et al (2013) Prevalence of endometriosis diagnosed by laparoscopy in adolescents with dysmenorrhea or chronic pelvic pain: a systematic review. Hum Reprod Update 19:570–582. https://doi.org/10.1093/humupd/dmt016
Koolhaas JM, De Boer SF, De Rutter AJ et al (1997) Social stress in rats and mice. Acta Physiol Scand Suppl 640:69–72
Koster R, Anderson M and De Beer EJ (1959) Acetic Acid for Analgesic Screening. Federation Proceedings 18:412–417
Laganà AS, Condemi I, Retto G et al (2015) Analysis of psychopathological comorbidity behind the common symptoms and signs of endometriosis. Eur J Obstet Gynecol Reprod Biol 194:30–33. https://doi.org/10.1016/j.ejogrb.2015.08.015
Laganà AS, Triolo O, Salmeri FM et al (2016) Natural killer T cell subsets in eutopic and ectopic endometrium: a fresh look to a busy corner. Arch Gynecol Obstet 293:941–949. https://doi.org/10.1007/s00404-015-4004-7
Laganà AS, Lucia V, Rosa L, et al (2017a) Anxiety and depression in patients with endometriosis : impact and management challenges. Int J Womens Health 9:323–330. https://doi.org/10.2147/IJWH.S119729
Laganà AS, Vitale SG, Salmeri FM et al (2017b) Unus pro omnibus, omnes pro uno: a novel, evidence-based, unifying theory for the pathogenesis of endometriosis. Med Hypotheses 103:10–20. https://doi.org/10.1016/j.mehy.2017.03.032
Latremoliere A, Woolf CJ (2009) Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J Pain 10:895–926. https://doi.org/10.1016/j.jpain.2009.06.012
Lee B-H, Kim Y-K (2010) The roles of BDNF in the pathophysiology of major depression and in antidepressant treatment. Psychiatry Investig 7:231–235. https://doi.org/10.4306/pi.2010.7.4.231
Lewter LA, Fisher JL, Siemian JN et al (2017) Antinociceptive effects of a novel α2/α3-subtype selective GABAA receptor positive allosteric modulator. ACS Chem Neurosci 8:1305–1312. https://doi.org/10.1021/acschemneuro.6b00447
Li S-X, Zhang J-C, Wu J, Hashimoto K (2014) Antidepressant effects of ketamine on depression-like behavior in juvenile mice after neonatal dexamethasone exposure. Clin Psychopharmacol Neurosci 12:124–127. https://doi.org/10.9758/cpn.2014.12.2.124
Li Y, Adur MK, Kannan A et al (2016) Progesterone alleviates endometriosis via inhibition of uterine cell proliferation, inflammation and angiogenesis in an immunocompetent mouse model. PLoS One 11:e0165347. https://doi.org/10.1371/journal.pone.0165347
Li T, Mamillapalli R, Ding S et al (2018) Endometriosis alters brain electro-physiology, gene expression and increased pain sensitization, anxiety, and depression in female mice‡. Biol Reprod 99:349–359. https://doi.org/10.1093/biolre/ioy035
Lima AP, Moura MD, Rosa e Silva AAM (2006) Prolactin and cortisol levels in women with endometriosis. Brazilian J Med Biol Res = Rev Bras Pesqui medicas e Biol 39:1121–1127
Lister RG (1987) The use of a plus-maze to measure anxiety in the mouse. Psychopharmacology 92:180–185
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275. https://doi.org/10.1016/0304-3894(92)87011-4
Lucca G, Comim CM, Valvassori SS et al (2009) Effects of chronic mild stress on the oxidative parameters in the rat brain. Neurochem Int 54:358–362. https://doi.org/10.1016/j.neuint.2009.01.001
Maes M, Galecki P, Chang YS, Berk M (2011) A review on the oxidative and nitrosative stress (O&NS) pathways in major depression and their possible contribution to the (neuro)degenerative processes in that illness. Prog Neuro-Psychopharmacol Biol Psychiatry 35:676–692. https://doi.org/10.1016/j.pnpbp.2010.05.004
Mara A, De CR, Freire L et al (2018) Chemico-biological interactions Antinociceptive activity of Riparin II from Aniba riparia : further elucidation of the possible mechanisms. Chem Biol Interact 287:49–56. https://doi.org/10.1016/j.cbi.2018.04.003
Marrocco J, Reynaert M-L, Gatta E et al (2014) The effects of antidepressant treatment in prenatally stressed rats support the glutamatergic hypothesis of stress-related disorders. J Neurosci 34:2015–2024. https://doi.org/10.1523/JNEUROSCI.4131-13.2014
Mattingly D (1962) A simple fluorometric method for the estimation of free 11-hydroxycorticoids in human plasma. J Clin Pathol 15:374–379
Mazereeuw G, Herrmann N, Andreazza AC et al (2015) A meta-analysis of lipid peroxidation markers in major depression. Neuropsychiatr Dis Treat 11:2479–2491. https://doi.org/10.2147/NDT.S89922
McAllister SL, McGinty KA, Resuehr D, Berkley KJ (2009) Endometriosis-induced vaginal hyperalgesia in the rat: role of the ectopic growths and their innervation. Pain 147:255–264. https://doi.org/10.1016/j.pain.2009.09.022
Mello BSF, Monte AS, McIntyre RS et al (2013) Effects of doxycycline on depressive-like behavior in mice after lipopolysaccharide (LPS) administration. J Psychiatr Res 47:1521–1529. https://doi.org/10.1016/j.jpsychires.2013.06.008
Mello BSF, Chaves Filho AJM, Custódio CS et al (2018) Sex influences in behavior and brain inflammatory and oxidative alterations in mice submitted to lipopolysaccharide-induced inflammatory model of depression. J Neuroimmunol 320:133–142. https://doi.org/10.1016/j.jneuroim.2018.04.009
MMed ML, Liu X, Zhang Y, Guo S-W (2012) Valproic acid and progestin inhibit lesion growth and reduce hyperalgesia in experimentally induced endometriosis in rats. Reprod Sci 19:360–373. https://doi.org/10.1177/1933719111424453
Moretti M, Budni J, dos Santos DB et al (2013) Protective effects of ascorbic acid on behavior and oxidative status of restraint-stressed mice. J Mol Neurosci 49:68–79. https://doi.org/10.1007/s12031-012-9892-4
Moylan S, Berk M, Dean OM et al (2014) Oxidative & nitrosative stress in depression: why so much stress? Neurosci Biobehav Rev 45:46–62. https://doi.org/10.1016/j.neubiorev.2014.05.007
Murakami S, Imbe H, Morikawa Y, Kubo C, Senba E (2005) Chronic stress, as well as acute stress, reduces BDNF mRNA expression in the rat hippocampus but less robustly. Neurosci Res 53:129–139. https://doi.org/10.1016/j.neures.2005.06.008
Mutso AA, Petre B, Huang L et al (2014) Reorganization of hippocampal functional connectivity with transition to chronic back pain. J Neurophysiol 111:1065–1076. https://doi.org/10.1152/jn.00611.2013
Nasiri N, Moini A, Eftekhari-Yazdi P et al (2017) Oxidative stress statues in serum and follicular fluid of women with endometriosis. Cell J 18:582–587. https://doi.org/10.22074/CELLJ.2016.4724
Ngô C, Chéreau C, Nicco C et al (2009) Reactive oxygen species controls endometriosis progression. Am J Pathol 175:225–234. https://doi.org/10.2353/ajpath.2009.080804
NIH (2011) Guide for the care and use of laboratory animals. National Academies Press, Washington, D.C
O’Mahony CM, Clarke G, Gibney S et al (2011) Strain differences in the neurochemical response to chronic restraint stress in the rat: relevance to depression. Pharmacol Biochem Behav 97:690–699. https://doi.org/10.1016/j.pbb.2010.11.012
Pattison DI, Davies MJ, Hawkins CL (2012) Reactions and reactivity of myeloperoxidase-derived oxidants: differential biological effects of hypochlorous and hypothiocyanous acids. Free Radic Res 46:975–995. https://doi.org/10.3109/10715762.2012.667566
Pelch KE, Schroder AL, Kimball PA et al (2010) Aberrant gene expression profile in a mouse model of endometriosis mirrors that observed in women. Fertil Steril 93:1615–1627. https://doi.org/10.1016/j.fertnstert.2009.03.086
Pelch KE, Sharpe-Timms KL, Nagel SC (2012) Mouse model of surgically-induced endometriosis by auto-transplantation of uterine tissue. J Vis Exp:1–8. https://doi.org/10.3791/3396
Pope CJ, Sharma V, Sharma S, Mazmanian D (2015) WOMEN ’ S HEALTH a systematic review of the association between psychiatric disturbances and endometriosis. J Obstet Gynaecol Canada 37:1006–1015. https://doi.org/10.1016/S1701-2163(16)30050-0
Porsolt RD, Le Pichon M, Jalfre M (1977) Depression: a new animal model sensitive to antidepressant treatments. Nature 266:730–732
Pulli B, Ali M, Forghani R et al (2013) Measuring myeloperoxidase activity in biological samples. PLoS One 8:e67976. https://doi.org/10.1371/journal.pone.0067976
Qu Y, Yang C, Ren Q et al (2017) Comparison of (R)-ketamine and lanicemine on depression-like phenotype and abnormal composition of gut microbiota in a social defeat stress model. Sci Rep 7:15725. https://doi.org/10.1038/s41598-017-16060-7
Réus GZ, Abelaira HM, Maciel AL et al (2014) Minocycline protects against oxidative damage and alters energy metabolism parameters in the brain of rats subjected to chronic mild stress. Metab Brain Dis 30:545–553. https://doi.org/10.1007/s11011-014-9602-8
Russo AJ (2010) Increased serum cu/Zn SOD in individuals with clinical depression normalizes after zinc and anti-oxidant therapy. Nutr Metab Insights 3:37–42. https://doi.org/10.4137/NMI.S5044
Scutiero G, Iannone P, Bernardi G, et al (2017) Oxidative stress and endometriosis : A systematic review of the literature. Oxid Med Cell Longev 2017:7265238. https://doi.org/10.1155/2017/7265238
Sedlak J, Lindsay RH (1968) Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem 25:192–205
Sepulcri RP, do Amaral VF (2009) Depressive symptoms, anxiety, and quality of life in women with pelvic endometriosis. Eur J Obstet Gynecol Reprod Biol 142:53–56. https://doi.org/10.1016/j.ejogrb.2008.09.003
Sharpe-Timms KL (2002) Using rats as a research model for the study of endometriosis. Ann N Y Acad Sci 955:318–327; discussion 340–2, 396–406
Silva MCC, de Sousa CNS, Gomes PXL et al (2016) Evidence for protective effect of lipoic acid and desvenlafaxine on oxidative stress in a model depression in mice. Prog Neuro-Psychopharmacol Biol Psychiatry 64:142–148. https://doi.org/10.1016/j.pnpbp.2015.08.002
Simsek Y, Gul M, Yilmaz E et al (2014) Atorvastatin exerts anti-nociceptive activity and decreases serum levels of high-sensitivity C-reactive protein and tumor necrosis factor-α in a rat endometriosis model. Arch Gynecol Obstet 290:999–1006. https://doi.org/10.1007/s00404-014-3295-4
Soliman AM, Yang H, Du EX et al (2016) The direct and indirect costs associated with endometriosis: a systematic literature review. Hum Reprod 31:712–722. https://doi.org/10.1093/humrep/dev335
Souza CA, Oliveira LM, Scheffel C et al (2011) Quality of life associated to chronic pelvic pain is independent of endometriosis diagnosis-a cross-sectional survey. Health Qual Life Outcomes 9:41. https://doi.org/10.1186/1477-7525-9-41
Sun Y, Oberley LW, Li Y (1988) A simple method for clinical assay of superoxide dismutase. Clin Chem 34:497–500
Suzuki K, Ota H, Sasagawa S et al (1983) Assay method for myeloperoxidase in human polymorphonuclear leukocytes. Anal Biochem 132:345–352. https://doi.org/10.1016/0003-2697(83)90019-2
Talarowska M, Szemraj J, Gałecki P (2015) Myeloperoxidase gene expression and cognitive functions in depression. Adv Med Sci 60:1–5. https://doi.org/10.1016/j.advms.2014.06.001
Tariverdian N, Rücke M, Szekeres-Bartho J et al (2010) Neuroendocrine circuitry and endometriosis: progesterone derivative dampens corticotropin-releasing hormone-induced inflammation by peritoneal cells in vitro. J Mol Med 88:267–278. https://doi.org/10.1007/s00109-009-0559-8
Tirado-González I, Barrientos G, Tariverdian N et al (2010) Endometriosis research: animal models for the study of a complex disease. J Reprod Immunol 86:141–147. https://doi.org/10.1016/j.jri.2010.05.001
Tomaz VS, Cordeiro RC, Costa AMN et al (2014) Antidepressant-like effect of nitric oxide synthase inhibitors and sildenafil against lipopolysaccharide-induced depressive-like behavior in mice. Neuroscience 268:236–246. https://doi.org/10.1016/j.neuroscience.2014.03.025
Torres-Reverón A, Rivera-Lopez LL, Flores I, Appleyard CB (2018) Antagonizing the corticotropin releasing hormone receptor 1 with antalarmin reduces the progression of endometriosis. PLoS One 13:e0197698. https://doi.org/10.1371/journal.pone.0197698
Tsai M-C, Huang T-L (2016) Increased activities of both superoxide dismutase and catalase were indicators of acute depressive episodes in patients with major depressive disorder. Psychiatry Res 235:38–42. https://doi.org/10.1016/j.psychres.2015.12.005
Túnez I, Drucker-Colín R, Montilla P et al (2010) Protective effect of nicotine on oxidative and cell damage in rats with depression induced by olfactory bulbectomy. Eur J Pharmacol 627:115–118. https://doi.org/10.1016/j.ejphar.2009.10.061
Vaccarino V, Brennan M-L, Miller AH et al (2008) Association of major depressive disorder with serum myeloperoxidase and other markers of inflammation: a twin study. Biol Psychiatry 64:476–483. https://doi.org/10.1016/j.biopsych.2008.04.023
Vernon MW, Wilson EA (1985) Studies on the surgical induction of endometriosis in the rat. Fertil Steril 44:684–694
Vetvicka V, Laganà AS, Salmeri FM et al (2016) Regulation of apoptotic pathways during endometriosis: from the molecular basis to the future perspectives. Arch Gynecol Obstet 294:897–904. https://doi.org/10.1007/s00404-016-4195-6
Vitale SG, La Rosa VL, Rapisarda AMC, Laganà AS (2017) Impact of endometriosis on quality of life and psychological well-being. J Psychosom Obstet Gynecol 38:317–319. https://doi.org/10.1080/0167482X.2016.1244185
Vitale SG, Capriglione S, Peterlunger I et al (2018) The role of oxidative stress and membrane transport systems during endometriosis: a fresh look at a busy corner. Oxidative Med Cell Longev 2018:7924021. https://doi.org/10.1155/2018/7924021
Walker AK, Kavelaars A, Heijnen CJ, Dantzer R (2014) Neuroinflammation and comorbidity of pain and depression. Pharmacol Rev 66:80–101. https://doi.org/10.1124/pr.113.008144
Wickström K, Edelstam G (2017) Minimal clinically important difference for pain on the VAS scale and the relation to quality of life in women with endometriosis. Sex Reprod Healthc 13:35–40. https://doi.org/10.1016/j.srhc.2017.05.004
Willner P (2005) Chronic mild stress (CMS) revisited: consistency and behavioural-neurobiological concordance in the effects of CMS. Neuropsychobiology 52:90–110. https://doi.org/10.1159/000087097
Willner P (2017) The chronic mild stress (CMS) model of depression: history, evaluation and usage. Neurobiol Stress 6:78–93. https://doi.org/10.1016/j.ynstr.2016.08.002
Xu B, Gottschalk W, Chow A et al (2000) The role of brain-derived neurotrophic factor receptors in the mature hippocampus: modulation of long-term potentiation through a presynaptic mechanism involving TrkB. J Neurosci 20:6888–6897 doi: 20/18/6888 [pii]
Young E, Lopez JF, Murphy-Weinberg V et al (2000) Hormonal evidence for altered responsiveness to social stress in major depression. Neuropsychopharmacology 23:411–418. https://doi.org/10.1016/S0893-133X(00)00129-9
Yuan M, Li D, An M et al (2016) Rediscovering peritoneal macrophages in a murine endometriosis model. Hum Reprod 32:94–102. https://doi.org/10.1093/humrep/dew274
Acknowledgements
The authors thank Ms. Maria Vilani for technical support.
Role of funding source
This work was partially supported by CNPq and CAPES.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest for the present investigation.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Paulo Wagner Linhares Lima Filho and Adriano José Maia Chaves Filho should be considered co-first authors
Highlights
- Endometriosis model (EM) is related to several features of clinical depression;
- EM causes progressive increases in anxiety-like behavior;
- Behavioral alterations followed the cystic growth of endometriosis lesions;
- Hippocampal oxidative and neurotrophic changes underlie EM behavioral alterations
Rights and permissions
About this article
Cite this article
Filho, P.W.L.L., Chaves Filho, A.J.M., Vieira, C.F.X. et al. Peritoneal endometriosis induces time-related depressive- and anxiety-like alterations in female rats: involvement of hippocampal pro-oxidative and BDNF alterations. Metab Brain Dis 34, 909–925 (2019). https://doi.org/10.1007/s11011-019-00397-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11011-019-00397-1