Metabolic Brain Disease

, Volume 34, Issue 3, pp 909–925 | Cite as

Peritoneal endometriosis induces time-related depressive- and anxiety-like alterations in female rats: involvement of hippocampal pro-oxidative and BDNF alterations

  • Paulo Wagner Linhares Lima Filho
  • Adriano José Maia Chaves Filho
  • Charliene Freire Xavier Vieira
  • Tatiana de Queiroz Oliveira
  • Michelle Verde Ramo Soares
  • Paloma Marinho Jucá
  • Joao Quevedo
  • Tatiana Barichello
  • Danielle MacedoEmail author
  • Francisco das Chagas Medeiros
Original Article


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.


Endometriosis Depression Animal models Hippocampus Oxidative stress Brain-derived-neurotrophic factor 



The authors thank Ms. Maria Vilani for technical support.

Role of funding source

This work was partially supported by CNPq and CAPES.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest for the present investigation.


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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Paulo Wagner Linhares Lima Filho
    • 1
    • 3
  • Adriano José Maia Chaves Filho
    • 1
  • Charliene Freire Xavier Vieira
    • 1
  • Tatiana de Queiroz Oliveira
    • 1
  • Michelle Verde Ramo Soares
    • 1
  • Paloma Marinho Jucá
    • 1
  • Joao Quevedo
    • 4
    • 5
    • 6
  • Tatiana Barichello
    • 4
    • 5
    • 6
  • Danielle Macedo
    • 1
    • 2
    Email author
  • Francisco das Chagas Medeiros
    • 3
  1. 1.Neuropsychopharmacology Laboratory, Drug Research and Development Center, Faculty of Medicine, Department of Physiology and PharmacologyUniversidade Federal do CearáFortalezaBrazil
  2. 2.National Institute for Translational Medicine (INCT-TM, CNPq)Ribeirão PretoBrazil
  3. 3.Surgery Department, Faculty of MedicineUniversidade Federal do CearáFortalezaBrazil
  4. 4.Translational Psychiatry Program, Department of Psychiatry and Behavioral Sciences, McGovern Medical SchoolThe University of Texas Health Science Center at HoustonHoustonUSA
  5. 5.Center of Excellence on Mood Disorders, Department of Psychiatry and Behavioral Sciences, McGovern Medical SchoolThe University of Texas Health Science Center at HoustonHoustonUSA
  6. 6.Laboratory of Neurosciences, Graduate Program in Health SciencesUniversity of Southern Santa Catarina – UNESCCriciúmaBrazil

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