Pathogenesis and pathophysiology of endometriosis

Burney, Richard O.; Giudice, Linda C.

doi:10.1016/j.fertnstert.2012.06.029

Cited by 1,590Endometriosis Research and TreatmentGynecological conditions and treatmentsEctopic Pregnancy Diagnosis and Management

Pathogenesis and pathophysiology of endometriosis

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Burney, Richard O., Giudice, Linda C.·2012·Fertility and Sterility

DOI 10.1016/j.fertnstert.2012.06.029PMC PMC3836682

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Abstract

Originally described over three hundred years ago, endometriosis is classically defined by the presence of endometrial glands and stroma in extrauterine locations. Endometriosis is an inflammatory, estrogen-dependent condition associated with pelvic pain and infertility. This work reviews the disease process from theories regarding origin to the molecular basis for disease sequelae. A thorough understanding of the histopathogenesis and pathophysiology of endometriosis is essential to the development of novel diagnostic and treatment approaches for this debilitating condition.

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Loss of progesterone responsiveness leads to increased growth of endometriotic lesions and a non-receptive endometrium.
“Since P4 signaling is required to counteract E2-induced proliferation and to promote decidualization [55], the loss of P4-responsiveness leads to both an increased growth of endometriotic lesions and to a non-receptive endometrium [33, 56].”
From Hormonal treatments for endometriosis: The endocrine background (2022) · cites this paper as [56]
In “Altered hormonal milieu: estrogen dependence and progesterone resistance” (page unavailable), the paper links progesterone resistance and incomplete secretory transition to enhanced survival and implantation of refluxed endometrium. “Endometrial cell attachment and invasion” (page unavailable) reports that progesterone failed to prevent transplanted endometrium from establishing disease in mice. These passages support a role in lesion establishment, but do not establish increased growth of existing lesions or explicitly describe the uterine endometrium as non-receptive. (LLM, conf=0.85)
Experimental — accuracy not yet measured
Scar endometriosis is a challenging diagnosis to establish because it is reached by exclusion rather than as a positive diagnosis process, due to non-specificity of symptoms such as cyclic abdominal pain, swelling, or bruising of the scar post-surgery.
“Scar endometriosis is a challenging diagnosis to establish because it is reached rather by exclusion than as a positive diagnosis process. This is due to the non-specificity of symptoms such as cyclic abdominal pain, swelling, or bruising of the scar post-surgery.”
From Abdominal Wall Endometriosis: Two Case Reports and Literature Review (2020) · cites this paper as [4]
Preoperative evaluation of invasion is very important because in case of large muscle invasion or deep invasion into omentum or bowel, participation of a general surgeon is necessary.
“Preoperative evaluation of invasion is very important because, in case of large muscle invasion or deep invasion into the omentum or bowel, the participation of a general surgeon is necessary, with all the logistical implications [4].”
From Abdominal Wall Endometriosis: Two Case Reports and Literature Review (2020) · cites this paper as [4]
Ultrasound may be useful for preoperative diagnosis and evaluation of invasion into subjacent anatomical planes in scar endometriosis.
“The ultrasound may be useful for preoperative diagnosis and evaluation of invasion into the subjacent anatomical planes.”
From Abdominal Wall Endometriosis: Two Case Reports and Literature Review (2020) · cites this paper as [4]
Symptoms occur after puberty and oestrogen action contributes to pathological processes including growth of lesions and inflammation, and to symptoms including pain.
“Symptoms occur after puberty and oestrogen action contributes to pathological processes including growth of lesions and inflammation, and to the symptoms including pain4142.”
From Meta-analysis identifies five novel loci associated with endometriosis highlighting key genes involved in hormone metabolism (2017) · cites this paper as [42]

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Retracted
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Yang, Y., Degranpré, P., Kharfi, A., & Akoum, A. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.12.7003 · Cited by 92 · see citing works
Stenosis of the external cervical os: an association with endometriosis in women with chronic pelvic pain
Barbieri, R. L. (1998) · Fertility and Sterility · doi:10.1016/s0015-0282(98)00189-7 · Cited by 92 · see citing works
Endometrial induction of endometriosis across Millipore filters.
Merrill, J. A. (1966) · PubMed · Cited by 88 · see citing works
Marked elevation of macrophage migration inhibitory factor in the peritoneal fluid of women with endometriosis
Kats, R., Collette, T., Metz, C. N., & Akoum, A. (2002) · Fertility and Sterility · doi:10.1016/s0015-0282(02)03189-8 · Cited by 83 · see citing works
Macrophage migration inhibitory factor expression in the intrauterine endometrium of women with endometriosis varies with disease stage, infertility status, and pelvic pain
Akoum, A., Metz, C. N., Al-Akoum, M., & Kats, R. (2006) · Fertility and Sterility · doi:10.1016/j.fertnstert.2005.10.073 · Cited by 78 · see citing works
Pelvic peritoneal defects and endometriosis: Allen-Masters syndrome revisited
Chatman, D. L. (1981) · Fertility and Sterility · doi:10.1016/s0015-0282(16)45921-2 · Cited by 76 · see citing works
Is there an association between septate uterus and endometriosis?
Nawroth, F., Rahimi, G., Nawroth, C., Foth, D., Ludwig, M., & Schmidt, T. (2006) · Human Reproduction · doi:10.1093/humrep/dei344 · Cited by 70 · see citing works
Autoantibodies and infertility: a review of the literature
Voorhis, B. J. V., & Stovall, D. W. (1997) · Journal of Reproductive Immunology · doi:10.1016/s0165-0378(97)00025-9 · Cited by 69 · see citing works
Modulation of NK Cell Lytic Function by Endometrial Secretory Factors: Potential Role in Endometriosis
Somigliana, E., Viganò, P., Gaffuri, B., Candiani, M., Busacca, M., Blasio, A. M. D., & Vignali, M. (1996) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.1996.tb00179.x · Cited by 65 · see citing works
Increased secretion of hepatocyte growth factor by eutopic endometrial stromal cells in women with endometriosis
Sugawara, J., Fukaya, T., Murakami, T., Yoshida, H., & Yajima, A. (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)00226-4 · Cited by 64 · see citing works
The insulin-like growth factor system in human peritoneal fluid: its effects on endometrial stromal cells and its potential relevance to endometriosis
Giudice, L. C., Dsupin, B. A., Gargosky, S. E., Rosenfeld, R. G., & Irwin, J. C. (1994) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.79.5.7525631 · Cited by 62 · see citing works
Self-citation
Endometriotic Lesions Synthesize and Secrete a Haptoglobin-Like Protein1
Sharpe-Timms, K. L., Piva, M. A., Ricke, E. A., Surewicz, K. A., Zhang, Y. L., & Zimmer, R. L. (1998) · Biology of Reproduction · doi:10.1095/biolreprod58.4.988 · Cited by 61 · see citing works
Three-dimensional architectures of peritoneal endometriosis
Donnez, J., Nisolle, M., & Casanas‐Roux, F. (1992) · Fertility and Sterility · doi:10.1016/s0015-0282(16)55012-2 · Cited by 60 · see citing works
Aberrant portions of the müllerian duct found in an ovary
Russell, W. (1979) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(79)90890-1 · Cited by 60 · see citing works
Genomic Alterations in Ectopic and Eutopic Endometria of Women with Endometriosis
Wu, Y., Strawn, E., Basir, Z., Wang, Y., Halverson, G., Jailwala, P., & Guo, S. (2006) · Gynecologic and Obstetric Investigation · doi:10.1159/000093130 · Cited by 58 · see citing works
Stimulation of prostaglandin (PG) F2α and PGE2 release by tumour necrosis factor-α and interleukin-1α in cultured human luteal phase endometrial cells
Chen, D.-B., Yang, Z., Le, S.-P., & Harper, M. J. K. (1995) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a135790 · Cited by 57 · see citing works
Tissue integrity is essential for ectopic implantation of human endometrium in the chicken chorioallantoic membrane
Nap, A. W., Groothuis, P. G., Demir, A. Y., Maas, J. W. M., Dunselman, G. A. J., de Goeij, A. F. P. M., & Evers, J. L. H. (2003) · Human Reproduction · doi:10.1093/humrep/deg033 · Cited by 55 · see citing works
Endometriosis in a patient with Rokitansky-Kuster-Hauser syndrome
Rosenfeld, D. L., & Lecher, B. D. (1981) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(81)90418-x · Cited by 51 · see citing works
Left Lateral Predisposition of Endometriosis and Endometrioma
Al-Fozan, H. M., & Tulandi, T. (2003) · Obstetrics and Gynecology · doi:10.1097/00006250-200301000-00030 · Cited by 50 · see citing works
Epidermal growth factor and basic fibroblast growth factor in peritoneal fluid of women with endometriosis
Huang, J.-C., Papasakelariou, C., & Dawood, M. Y. (1996) · Fertility and Sterility · doi:10.1016/s0015-0282(16)58263-6 · Cited by 47 · see citing works
Genomic alterations in the endometrium may be a proximate cause for endometriosis
Guo, S., Wu, Y., Strawn, E., Basir, Z., Wang, Y., Halverson, G., Montgomery, K., & Kajdacsy-Balla, A. (2004) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2004.02.004 · Cited by 46 · see citing works
Current concepts on pathology, histogenesis and etiology of endometriosis
Dmowski, W. P., & Radwańska, E. (1984) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.3109/00016348409156978 · Cited by 42 · see citing works
Elevated angiogenin levels in the peritoneal fluid of women with endometriosis correlate with the extent of the disorder
Suzumori, N., Zhao, X. X., & Suzumori, K. (2004) · Fertility and Sterility · doi:10.1016/j.fertnstert.2003.11.043 · Cited by 41 · see citing works
Induction of endometrial epithelial cell invasion and c-fms expression by transforming growth factor beta
Liu, Y.-G., TEKMAL, R. R., Binkley, P. A., Nair, H. B. B., Schenken, R. S., & Kirma, N. B. (2009) · Molecular Human Reproduction · doi:10.1093/molehr/gap043 · Cited by 36 · see citing works
Expression of Platelet-Derived Endothelial Cell Growth Factor (PD-ECGF) Related to Angiogenesis in Ovarian Endometriosis
Fujimoto, J., Sakaguchi, H., Hirose, R., & Tamaya, T. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.84.1.5372 · Cited by 35 · see citing works
Endometrial Stromal Cells and Immune Cell Populations Within Lymph Nodes in a Nonhuman Primate Model of Endometriosis
Hey-Cunningham, A. J., Fazleabas, A. T., Braundmeier, A. G., Markham, R., Fraser, I. S., & Berbic, M. (2011) · Reproductive Sciences · doi:10.1177/1933719110397210 · Cited by 30 · see citing works
Menstrual bleeding from an endometriotic lesion
Burney, R. O., & Lathi, R. B. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.08.125 · Cited by 27 · see citing works
Self-citation
On the Vasculature of Ectopic Endometrium with Decidual Reaction
Nieminen, U. (1963) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.3109/00016346309157877 · Cited by 4 · see citing works

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Endometriosis: pathogenesis and treatment
Vercellini, P., Viganò, P., Somigliana, E., & Fedele, L. (2014) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2013.255 · Cited by 1,940 · see citing works
Endometriosis: Epidemiology, Classification, Pathogenesis, Treatment and Genetics (Review of Literature)
Smolarz, B., Szyłło, K., & Romanowicz, H. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms221910554 · Cited by 560 · see citing works
Theories on the pathogenesis of endometriosis
Sourial, S., Tempest, N., & Hapangama, D. K. (2014) · International Journal of Reproductive Medicine · doi:10.1155/2014/179515 · Cited by 418 · see citing works
The Burden of Endometriosis on Women’s Lifespan: A Narrative Overview on Quality of Life and Psychosocial Wellbeing
Della Corte, L., Di Filippo, C., Gabrielli, O., Reppuccia, S., La Rosa, V. L., Ragusa, R., Fichera, M., Commodari, E., Bifulco, G., & Giampaolino, P. (2020) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph17134683 · Cited by 387 · see citing works
Meta-analysis identifies five novel loci associated with endometriosis highlighting key genes involved in hormone metabolism
Sapkota, Y., Steinthorsdottir, V., Morris, A. P., Fassbender, A., Rahmioglu, N., De Vivo, I., Buring, J. E., Zhang, F., Edwards, T. L., Jones, S., et al. (2017) · Nature Communications · doi:10.1038/ncomms15539 · Cited by 344 · see citing works
Hormonal treatments for endometriosis: The endocrine background
Vannuccini, S., Clemenza, S., Rossi, M., & Petraglia, F. (2022) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-021-09666-w · Cited by 336 · see citing works
“Since P4 signaling is required to counteract E2-induced proliferation and to promote decidualization [55], the loss of P4-responsiveness leads to both an increased growth of endometriotic lesions and to a non-receptive endometrium [33, 56].”
Background
Biomarkers in endometriosis: Challenges and opportunities
Ahn, S. H., Singh, V., & Tayade, C. (2017) · Fertility and Sterility · doi:10.1016/j.fertnstert.2017.01.009 · Cited by 242 · see citing works
Unus pro omnibus, omnes pro uno: a novel, evidence-based, unifying theory for the pathogenesis of endometriosis
Laganà, A. S., Vitale, S. G., Salmeri, F. M., Triolo, O., Ban Frangež, H., Vrtačnik-Bokal, E., Stojanovska, L., Apostolopoulos, V., Granese, R., & Sofo, V. (2017) · Medical Hypotheses · doi:10.1016/j.mehy.2017.03.032 · Cited by 221 · see citing works
Genome-wide DNA methylation analysis predicts an epigenetic switch for GATA factor expression in endometriosis
Dyson, M. T., Roqueiro, D., Monsivais, D., Ercan, C. M., Pavone, M. E., Brooks, D. C., Kakinuma, T., Ono, M., Jafari, N., Dai, Y., et al. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004158 · Cited by 211 · see citing works
Estradiol is a critical mediator of macrophage-nerve cross talk in peritoneal endometriosis
Greaves, E., Temp, J., Esnal-Zufiurre, A., Mechsner, S., Horne, A. W., & Saunders, P. T. K. (2015) · The American Journal of Pathology · doi:10.1016/j.ajpath.2015.04.012 · Cited by 201 · see citing works
Peripheral changes in endometriosis-associated pain
Morotti, M., Vincent, K., Brawn, J., Zondervan, K. T., & Becker, C. M. (2014) · Human Reproduction Update · doi:10.1093/humupd/dmu021 · Cited by 198 · see citing works
Bacterial contamination hypothesis: a new concept in endometriosis
Khan, K. N., Fujishita, A., Hiraki, K., Kitajima, M., Nakashima, M., Fushiki, S., & Kitawaki, J. (2018) · Reproductive Medicine and Biology · doi:10.1002/rmb2.12083 · Cited by 176 · see citing works
Human Endometrial Fibroblasts Derived from Mesenchymal Progenitors Inherit Progesterone Resistance and Acquire an Inflammatory Phenotype in the Endometrial Niche in Endometriosis1
Barragan, F., Irwin, J. C., Balayan, S., Erikson, D. W., Chen, J. C., Houshdaran, S., Piltonen, T. T., Spitzer, T. L. B., George, A., Rabban, J. T., et al. (2016) · Biology of Reproduction · doi:10.1095/biolreprod.115.136010 · Cited by 152 · see citing works
Self-citation
MicroRNA expression profile in endometriosis: its relation to angiogenesis and fibrinolytic factors
Braza-Boïls, A., Marí-Alexandre, J., Gilabert, J., Sánchez-Izquierdo, D., España, F., Estellés, A., & Gilabert-Estellés, J. (2014) · Human Reproduction · doi:10.1093/humrep/deu019 · Cited by 164 · see citing works
The Pathogenesis of Adenomyosis vis-à-vis Endometriosis
Guo, S.-W. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9020485 · Cited by 165 · see citing works
“For endometriosis, several theories regarding its pathogenesis have been proposed, and these hypotheses can be divided into three themes: in situ development (such as coelomic metaplasia or embryonic cell rests), implantation, or a combination of in situ development and implantation [25,26].”
Background
The management of menopause in women with a history of endometriosis: A systematic review
Gemmell, L. C., Webster, K. E., Kirtley, S., Vincent, K., Zondervan, K. T., & Becker, C. M. (2017) · Human Reproduction Update · doi:10.1093/humupd/dmx011 · Cited by 154 · see citing works
Menstruation pulls the trigger for inflammation and pain in endometriosis
Laux-Biehlmann, A., d’Hooghe, T., & Zollner, T. M. (2015) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2015.03.004 · Cited by 150 · see citing works
Targeting Oxidative Stress Involved in Endometriosis and Its Pain
Clower, L., Fleshman, T., Geldenhuys, W. J., & Santanam, N. (2022) · Biomolecules · doi:10.3390/biom12081055 · Cited by 145 · see citing works
Current and emerging treatment options for endometriosis
Ferrero, S., Evangelisti, G., & Barra, F. (2018) · Expert Opinion on Pharmacotherapy · doi:10.1080/14656566.2018.1494154 · Cited by 152 · see citing works
Platelets are an unindicted culprit in the development of endometriosis: clinical and experimental evidence
Ding, D., Liu, X., Duan, J., & Guo, S.-W. (2015) · Human Reproduction · doi:10.1093/humrep/dev025 · Cited by 139 · see citing works
Long-Term Outcomes of Elagolix in Women With Endometriosis: Results From Two Extension Studies
Surrey, E., Taylor, H. S., Giudice, L., Lessey, B. A., Abrao, M. S., Archer, D. F., Diamond, M. P., Johnson, N. P., Watts, N. B., Gallagher, J. C., et al. (2018) · Obstetrics & Gynecology · doi:10.1097/aog.0000000000002675 · Cited by 139 · see citing works
Self-citation
Eutopic endometrium in women with endometriosis: ground zero for the study of implantation defects
Lessey, B., Lebovic, D., & Taylor, R. (2013) · Seminars in Reproductive Medicine · doi:10.1055/s-0032-1333476 · Cited by 113 · see citing works
Aberrant Endometrial DNA Methylome and Associated Gene Expression in Women with Endometriosis
Houshdaran, S., Nezhat, C. R., Vo, K. C., Zelenko, Z., Irwin, J. C., & Giudice, L. C. (2016) · Biology of Reproduction · doi:10.1095/biolreprod.116.140434 · Cited by 113 · see citing works
Self-citation
Current understanding on pharmacokinetics, clinical efficacy and safety of progestins for treating pain associated to endometriosis
Barra, F., Scala, C., & Ferrero, S. (2018) · Expert Opinion on Drug Metabolism & Toxicology · doi:10.1080/17425255.2018.1461840 · Cited by 100 · see citing works
Endometriosis and endometriosis-associated cancers: new insights into the molecular mechanisms of ovarian cancer development
Dawson, A., Llauradó Fernandez, M., Anglesio, M., Yong, P. J., & Carey, M. S. (2018) · ecancermedicalscience · doi:10.3332/ecancer.2018.803 · Cited by 106 · see citing works
DNA methylation in endometriosis (Review)
KOUKOURA, O., SIFAKIS, S., & SPANDIDOS, D. A. (2016) · Molecular Medicine Reports · doi:10.3892/mmr.2016.4925 · Cited by 103 · see citing works
Uncovering steroidopathy in women with autism: a latent class analysis
Pohl, A., Cassidy, S., Auyeung, B., & Baron-Cohen, S. (2014) · Molecular Autism · doi:10.1186/2040-2392-5-27 · Cited by 97 · see citing works
Pain Catastrophizing and Pain Health-Related Quality-of-Life in Endometriosis
McPeak, A. E., Allaire, C., Williams, C., Albert, A., Lisonkova, S., & Yong, P. J. (2018) · The Clinical Journal of Pain · doi:10.1097/ajp.0000000000000539 · Cited by 101 · see citing works
Hormonal therapy for endometriosis: from molecular research to bedside
Tosti, C., Biscione, A., Morgante, G., Bifulco, G., Luisi, S., & Petraglia, F. (2017) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2016.05.032 · Cited by 96 · see citing works
Endometriosis impairs bone marrow-derived stem cell recruitment to the uterus whereas bazedoxifene treatment leads to endometriosis regression and improved uterine stem cell engraftment
Sakr, S., Naqvi, H., Komm, B., & Taylor, H. S. (2014) · Endocrinology · doi:10.1210/en.2013-1977 · Cited by 91 · see citing works
Endometriosis and polycystic ovary syndrome are diametric disorders
Dinsdale, N. L., & Crespi, B. J. (2021) · Evolutionary Applications · doi:10.1111/eva.13244 · Cited by 90 · see citing works
“The etiology of endometriosis, a condition diagnosed when endometrial tissue proliferates beyond the uterine boundaries, is highly enigmatic (Bulun et al., 2019; Burney & Giudice, 2012; Giudice & Kao, 2004).”
Background
Self-management and psychological-sexological interventions in patients with endometriosis: strategies, outcomes, and integration into clinical care
Buggio, L., Barbara, G., Facchin, F., Frattaruolo, M. P., Aimi, G., & Berlanda, N. (2017) · International Journal of Women's Health · doi:10.2147/ijwh.s119724 · Cited by 85 · see citing works
Epigenetic alterations affecting transcription factors and signaling pathways in stromal cells of endometriosis
Yotova, I., Hsu, E., Do, C., Gaba, A., Sczabolcs, M., Dekan, S., Kenner, L., Wenzl, R., & Tycko, B. (2017) · PLOS ONE · doi:10.1371/journal.pone.0170859 · Cited by 81 · see citing works
Intra-tissue steroid profiling indicates differential progesterone and testosterone metabolism in the endometrium and endometriosis lesions
Huhtinen, K., Saloniemi-Heinonen, T., Keski-Rahkonen, P., Desai, R., Laajala, D., Ståhle, M., Häkkinen, M. R., Awosanya, M., Suvitie, P., Kujari, H., et al. (2014) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2014-1913 · Cited by 75 · see citing works
Neural involvement in endometriosis: Review of anatomic distribution and mechanisms
Siquara De Sousa, A. C., Capek, S., Amrami, K. K., & Spinner, R. J. (2015) · Clinical Anatomy · doi:10.1002/ca.22617 · Cited by 77 · see citing works
The role of gene polymorphisms in endometriosis
Matalliotakis, M., Zervou, M. I., Matalliotaki, C., Rahmioglu, N., Koumantakis, G., Kalogiannidis, I., Prapas, I., Zondervan, K., Spandidos, D. A., Matalliotakis, I., et al. (2017) · Molecular Medicine Reports · doi:10.3892/mmr.2017.7398 · Cited by 75 · see citing works
Occult microscopic endometriosis: undetectable by laparoscopy in normal peritoneum
Khan, K. N., Fujishita, A., Kitajima, M., Hiraki, K., Nakashima, M., & Masuzaki, H. (2014) · Human Reproduction · doi:10.1093/humrep/det438 · Cited by 72 · see citing works
From pathogenesis to clinical practice: Emerging medical treatments for endometriosis
Clemenza, S., Sorbi, F., Noci, I., Capezzuoli, T., Turrini, I., Carriero, C., Buffi, N., Fambrini, M., & Petraglia, F. (2018) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2018.01.021 · Cited by 63 · see citing works
Systems genetics view of endometriosis: a common complex disorder
Baranov, V. S., Ivaschenko, T. E., Liehr, T., & Yarmolinskaya, M. I. (2015) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2014.11.036 · Cited by 62 · see citing works
Anxiety, coping skills and hypothalamus-pituitary-adrenal (HPA) axis in patients with endometriosis
Quiñones, M., Urrutia, R., Torres-Reverón, A., Vincent, K., & Flores, I. (2015) · Journal of Reproductive Biology and Health · doi:10.7243/2054-0841-3-2 · Cited by 60 · see citing works
The known, the unknown and the future of the pathophysiology of endometriosis
Ochoa Bernal, M. A., & Fazleabas, A. T. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25115815 · Cited by 59 · see citing works
“The immune system is believed to play an important role in the pathophysiology of endometriosis [75].”
Background
Abdominal wall endometriosis: an update in clinical, imagistic features, and management options
Grigore, M., Socolov, D., Pavaleanu, I., Scripcariu, I., Grigore, A. M., & Micu, R. (2017) · Medical Ultrasonography · doi:10.11152/mu-1248 · Cited by 55 · see citing works
Noninvasive biomarkers of endometriosis: myth or reality?
Lanišnik Rižner, T. (2014) · Expert Review of Molecular Diagnostics · doi:10.1586/14737159.2014.899905 · Cited by 52 · see citing works
Candidate genes for age at menarche are associated with endometriosis
Ponomarenko, I., Reshetnikov, E., Polonikov, A., Verzilina, I., Sorokina, I., Elgaeva, E. E., Tsepilov, Y. A., Yermachenko, A., Dvornyk, V., & Churnosov, M. (2020) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2020.04.016 · Cited by 49 · see citing works
Role of thyroid dysimmunity and thyroid hormones in endometriosis
Peyneau, M., Kavian, N., Chouzenoux, S., Nicco, C., Jeljeli, M., Toullec, L., Reboul-Marty, J., Chenevier-Gobeaux, C., Reis, F. M., Santulli, P., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1820469116 · Cited by 50 · see citing works
Micrometastasis of endometriosis to distant organs in a murine model
Samani, E. N., Mamillapalli, R., Li, F., Mutlu, L., Hufnagel, D., Krikun, G., & Taylor, H. S. (2019) · Oncotarget · doi:10.18632/oncotarget.16889 · Cited by 51 · see citing works
Co-culture with macrophages enhances the clonogenic and invasion activity of endometriotic stromal cells
Chan, R. W. S., Lee, C., Ng, E. H. Y., & Yeung, W. S. B. (2017) · Cell Proliferation · doi:10.1111/cpr.12330 · Cited by 45 · see citing works
Functional evaluation of genetic variants associated with endometriosis near GREB1
Fung, J. N., Holdsworth-Carson, S. J., Sapkota, Y., Zhao, Z. Z., Jones, L., Girling, J. E., Paiva, P., Healey, M., Nyholt, D. R., Rogers, P. A. W., et al. (2015) · Human Reproduction · doi:10.1093/humrep/dev051 · Cited by 46 · see citing works
Prevalence of high-risk human papillomavirus infection in women with ovarian endometriosis
Heidarpour, M., Derakhshan, M., Derakhshan‐Horeh, M., Kheirollahi, M., & Dashti, S. (2017) · Journal of obstetrics and gynaecology research · doi:10.1111/jog.13188 · Cited by 49 · see citing works
Endometriosis and type 1 allergies/immediate type hypersensitivity: a systematic review
Bungum, H. F., Vestergaard, C., & Knudsen, U. B. (2014) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2014.04.025 · Cited by 48 · see citing works
On-label and off-label drug use in the treatment of endometriosis
Quaas, A. M., Weedin, E. A., & Hansen, K. R. (2015) · Fertility and Sterility · doi:10.1016/j.fertnstert.2015.01.006 · Cited by 45 · see citing works
Endometrial vezatin and its association with endometriosis risk
Holdsworth-Carson, S. J., Fung, J. N., Luong, H. T. T., Sapkota, Y., Bowdler, L. M., Wallace, L., Teh, W. T., Powell, J. E., Girling, J. E., Healey, M., et al. (2016) · Human Reproduction · doi:10.1093/humrep/dew047 · Cited by 41 · see citing works
Overall Adiposity, Adipose Tissue Distribution, and Endometriosis: A Systematic Review
Backonja, U., Buck Louis, G. M., & Lauver, D. R. (2016) · Nursing Research · doi:10.1097/nnr.0000000000000146 · Cited by 39 · see citing works
Gonadotropin-releasing hormone analogues for endometriosis
Veth, V. B., van de Kar, M. M., Duffy, J. M., van Wely, M., Mijatovic, V., & Maas, J. W. (2023) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd014788.pub2 · Cited by 39 · see citing works
Chronic Fatigue, Physical Impairments and Quality of Life in Women with Endometriosis: A Case-Control Study
Álvarez-Salvago, F., Lara-Ramos, A., Cantarero-Villanueva, I., Mazheika, M., Mundo-López, A., Galiano-Castillo, N., Fernández-Lao, C., Arroyo-Morales, M., Ocón-Hernández, O., & Artacho-Cordón, F. (2020) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph17103610 · Cited by 38 · see citing works
Dienogest for Treatment of Endometriosis in Women: A 28-Week, Open-Label, Extension Study
Yu, Q., Zhang, S., Li, H., Wang, P., Zvolanek, M., Ren, X., Dong, L., & Lang, J. (2019) · Journal of Women's Health · doi:10.1089/jwh.2018.7084 · Cited by 34 · see citing works
Aberrant expression and localization of deoxyribonucleic acid methyltransferase 3B in endometriotic stromal cells
Dyson, M. T., Kakinuma, T., Pavone, M. E., Monsivais, D., Navarro, A., Malpani, S. S., Ono, M., & Bulun, S. E. (2015) · Fertility and Sterility · doi:10.1016/j.fertnstert.2015.06.046 · Cited by 37 · see citing works
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BackgroundInfluential
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Authors: Burney, R. O., & Giudice, L. C.
Affiliations: Madigan Army Medical Center (US)
University of California, San Francisco (US)
Corresponding author: Giudice, Linda C.
ORCID: Burney, Richard O.
Giudice, Linda C.
Venue: Fertility and Sterility
Publisher: Elsevier BV
Published: 2012-09
Volume: 98
Issue: 3
Pages: 511-519
ISSN: 0015-0282 (ISSN-L)
DOI: 10.1016/j.fertnstert.2012.06.029
PMC: PMC3836682
OpenAlex: W2071667212
Cited by: 1,590
References: 105
Citations by year: 2026: 110 · 2025: 121 · 2024: 160 · 2023: 152 · 2022: 158 · 2021: 151 · 2020: 148 · 2019: 106 · 2018: 97 · 2017: 93 · 2016: 83 · 2015: 91 · 2014: 76 · 2013: 40 · 2012: 3
FWCI: 9.11
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Fertility and Sterility (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
eScholarship (California Digital Library) (submittedVersion)
Funders: National Institutes of Health
National Institute of Child Health and Human Development
Eunice Kennedy Shriver National Institute of Child Health and Human Development (U54HD055764, P50HD055764)
Topics: Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
Health Sciences › Medicine › Obstetrics and Gynecology › Gynecological conditions and treatments
Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Ectopic Pregnancy Diagnosis and Management
Keywords: endometriosis, pathogenesis, pathophysiology, estrogen dependence, inflammation, pelvic pain, infertility, histopathogenesis, molecular mechanisms
MeSH terms: Animals, Cell Adhesion, Cell Survival, Endometriosis, Endometrium, Female, Humans, Inflammation, Neovascularization, Physiologic

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