Imbalance between sympathetic and sensory innervation in peritoneal endometriosis

Arnold, Julia; Barcena de Arellano, Maria L.; Rüster, Carola; Vercellino, Giuseppe F.; Chiantera, Vito; Schneider, Achim; Mechsner, Sylvia

doi:10.1016/j.bbi.2011.08.004

Cited by 132Endometriosis Research and TreatmentPain Mechanisms and TreatmentsGastrointestinal motility and disorders

Imbalance between sympathetic and sensory innervation in peritoneal endometriosis

Arnold, Julia, Barcena de Arellano, Maria L., Rüster, Carola, Vercellino, Giuseppe F., Chiantera, Vito, Schneider, Achim, Mechsner, Sylvia·2012·Brain, Behavior, and Immunity

DOI 10.1016/j.bbi.2011.08.004

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Abstract

To investigate possible mechanisms of pain pathophysiology in patients with peritoneal endometriosis, a clinical study on sensory and sympathetic nerve fibre sprouting in endometriosis was performed. Peritoneal lesions (n=40) and healthy peritoneum (n=12) were immunostained and analysed with anti-protein gene product 9.5 (PGP 9.5), anti-substance P (SP) and anti-tyrosine hydroxylase (TH), specific markers for intact nerve fibres, sensory nerve fibres and sympathetic nerve fibres, respectively, to identify the ratio of sympathetic and sensory nerve fibres. In addition, immune cell infiltrates in peritoneal endometriotic lesions were analysed and the nerve growth factor (NGF) and interleukin (IL)-1β expression was correlate with the nerve fibre density. Peritoneal fluids from patients with endometriosis (n=40) and without endometriosis (n=20) were used for the in vitro neuronal growth assay. Cultured chicken dorsal root ganglia (DRG) and sympathetic ganglia were stained with anti-growth associated protein 43 (anti-GAP 43), anti-SP and anti-TH. We could detect an increased sensory and decreased sympathetic nerve fibres density in peritoneal lesions compared to healthy peritoneum. Peritoneal fluids of patients with endometriosis compared to patients without endometriosis induced an increased sprouting of sensory neurites from DRG and decreased neurite outgrowth from sympathetic ganglia. In conclusion, this study demonstrates an imbalance between sympathetic and sensory nerve fibres in peritoneal endometriosis, as well as an altered modulation of peritoneal fluids from patients with endometriosis on sympathetic and sensory innervation which might directly be involved in the maintenance of inflammation and pain.

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Deep endometriosis (DE) lesions are frequently hyperinnervated.
“More strikingly, DE lesions are frequently hyperinnervated29–34.”
From Neuropeptides Substance P and Calcitonin Gene Related Peptide Accelerate the Development and Fibrogenesis of Endometriosis (2019) · cites this paper as [34]
In human studies, there is an imbalance between sympathetic and sensory nerve fibres in peritoneal endometriosis as well as an altered modulation of peritoneal fluids from patients with endometriosis on sympathetic and sensory innervation, which might directly be involved in the maintenance of inflammation and pain.
“In human studies, it has been reported that there is an imbalance between sympathetic and sensory nerve fibres in peritoneal endometriosis as well as an altered modulation of peritoneal fluids from patients with endometriosis on sympathetic and sensory innervation, which might directly be involved in the maintenance of inflammation and pain.82”
From Defining Future Directions for Endometriosis Research: Workshop Report From the 2011 World Congress of Endometriosis in Montpellier, France (2013) · cites this paper as [82]
A key feature observed in endometriosis lesions is the increased density of sensory nerve fibers in proximity to immune cells such as mast cells.
“A key feature observed in endometriosis lesions is the increased density of sensory nerve fibers in proximity to immune cells such as mast cells [ 9 , 10 , 11 ].”
From The Histamine-Associated Inflammatory Landscape of Endometriosis: Molecular Profiling of HDC, HRH1-HRH4, and Cytokines Across Lesion Subtypes (2025) · cites this paper as [9]
Histamine release serves as a key interface between immune activation and nociceptive signaling.
“They also align with previous reports of increased mast cell density and degranulation within endometriotic lesions and their spatial association with sensory nerve fibers [ 9 , 11 , 22 ], suggesting that histamine release serves as a key interface between immune activation and nociceptive signaling.”
From The Histamine-Associated Inflammatory Landscape of Endometriosis: Molecular Profiling of HDC, HRH1-HRH4, and Cytokines Across Lesion Subtypes (2025) · cites this paper as [9]

Revised American Society for Reproductive Medicine classification of endometriosis: 1996
American Society for Reproductive Medicine (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)81391-x · Cited by 3,018 · see citing works
DIRECT EVIDENCE FOR NEUROGENIC INFLAMMATION AND ITS PREVENTION BY DENERVATION AND BY PRETREATMENT WITH CAPSAICIN
Jancsó, N. V., Jancsó‐Gábor, A., & Szolcsányi, J. (1967) · British Journal of Pharmacology and Chemotherapy · doi:10.1111/j.1476-5381.1967.tb01984.x · Cited by 1,100 · see citing works
Nerve growth factor regulates expression of neuropeptide genes in adult sensory neurons
Lindsay, R. M., & Harmar, A. J. (1989) · Nature · doi:10.1038/337362a0 · Cited by 941 · see citing works
Peripheral and central mechanisms of cutaneous hyperalgesia
Treede, R., Meyer, R. A., Raja, S. N., & Campbell, J. N. (1992) · Progress in Neurobiology · doi:10.1016/0301-0082(92)90027-c · Cited by 917 · see citing works
Autonomic innervation and regulation of the immune system (1987–2007)
Nance, D. M., & Sanders, V. M. (2007) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2007.03.008 · Cited by 855 · see citing works
The pivotal role of tumour necrosis factor α in the development of inflammatory hyperalgesia
Cunha, F. Q., Poole, S., Lorenzetti, B. B., & Ferreira, S. H. (1992) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.1992.tb14503.x · Cited by 792 · see citing works
Nerve growth factor contributes to the generation of inflammatory sensory hypersensitivity
Woolf, C. J., Safieh‐Garabedian, B., Ma, Q., Crilly, P. J., & Winter, J. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90366-2 · Cited by 695 · see citing works
Nociceptors Are Interleukin-1β Sensors
Binshtok, A. M., Wang, H., Zimmermann, K., Amaya, F., Vardeh, D., Shi, L., Brenner, G. J., Ji, R., Bean, B. P., Woolf, C. J., et al. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.3795-08.2008 · Cited by 664 · see citing works
Interleukin-1β as a potent hyperalgesic agent antagonized by a tripeptide analogue
Ferreira, S. H., Lorenzetti, B. B., Bristow, A. F., & Poole, S. (1988) · Nature · doi:10.1038/334698a0 · Cited by 624 · see citing works
Increased content and transport of substance P and calcitonin gene-related peptide in sensory nerves innervating inflamed tissue: Evidence for a regulatory function of nerve growth factor in vivo
Donnerer, J., Schuligoi, R., & Stein, C. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90237-v · Cited by 605 · see citing works
Contribution of interleukin‐1β to the inflammation‐induced increase in nerve growth factor levels and inflammatory hyperalgesia
Safieh‐Garabedian, B., Poole, S., Allchorne, A. J., Winter, J., & Woolf, C. J. (1995) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.1995.tb15035.x · Cited by 594 · see citing works
Nerve growth factor-induced hyperalgesia in the neonatal and adult rat
Lewin, G. R., Ritter, A., & Mendell, L. M. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-05-02136.1993 · Cited by 562 · see citing works
Association between endometriosis stage, lesion type, patient characteristics and severity of pelvic pain symptoms: a multivariate analysis of over 1000 patients
Vercellini, P., Fedele, L., Aimi, G., Pietropaolo, G., Consonni, D., & Crosignani, P. G. (2007) · Human Reproduction · doi:10.1093/humrep/del339 · Cited by 547 · see citing works
Intraneuronal Substance P Contributes to the Severity of Experimental Arthritis
Levine, J. D., Clark, R. A., Devor, M. G., Helms, C. A., Moskowitz, M. A., & Basbaum, A. I. (1984) · Science · doi:10.1126/science.6208609 · Cited by 524 · see citing works
Neuropeptides in the Respiratory Tract: Part I
Barnes, P. J., Baraniuk, J. N., & Belvisi, M. G. (1991) · American Review of Respiratory Disease · doi:10.1164/ajrccm/144.5.1187 · Cited by 453 · see citing works
Time elapsed from onset of symptoms to diagnosis of endometriosis in a cohort study of Brazilian women
Arruda, M. S. (2003) · Human Reproduction · doi:10.1093/humrep/deg136 · Cited by 373 · see citing works
Mast cells increase in tissues of neonatal rats injected with the nerve growth factor
Aloe, L., & Levi‐Montalcini, R. (1977) · Brain Research · doi:10.1016/0006-8993(77)90772-7 · Cited by 352 · see citing works
Treatment of Endometriosis
Olive, D. L., & Pritts, E. A. (2001) · New England Journal of Medicine · doi:10.1056/nejm200107263450407 · Cited by 340 · see citing works
Interleukin‐1: A possible role in the infertility associated with endometriosis
Fakih, H., Baggett, B., & Holtz, G. (1988) · International Journal of Gynecology & Obstetrics · doi:10.1016/0020-7292(88)90224-x · Cited by 319 · see citing works
Hyperalgesia, nerve infiltration and nerve growth factor expression in deep adenomyotic nodules, peritoneal and ovarian endometriosis
Anaf, V., Simon, P., El Nakadi, I., Fayt, I., Simonart, T., Buxant, F., & Noel, J.-C. (2002) · Human Reproduction · doi:10.1093/humrep/17.7.1895 · Cited by 317 · see citing works
Pathogenesis of endometriosis: natural immunity dysfunction or autoimmune disease?
Matarese, G., De Placido, G., Nikas, Y., & Alviggi, C. (2003) · Trends in Molecular Medicine · doi:10.1016/s1471-4914(03)00051-0 · Cited by 315 · see citing works
Estrogens and Autoimmune Diseases
Cutolo, M., Capellino, S., Sulli, A., SERIOLI, B., Secchi, M. E., Villaggio, B., & Straub, R. H. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1386.043 · Cited by 311 · see citing works
Increased activation of pelvic macrophages in infertile women with mild endometriosis
Halme, J. K., Becker, S., Hammond, M. G., Raj, M. H. G., & Raj, S. (1983) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(83)90720-2 · Cited by 305 · see citing works
Nerve fibres in peritoneal endometriosis
Tokushige, N., Markham, R., Russell, P., & Fraser, I. S. (2006) · Human Reproduction · doi:10.1093/humrep/del260 · Cited by 299 · see citing works
The loss of sympathetic nerve fibers in the synovial tissue of patients with rheumatoid arthritis is accompanied by increased norepinephrine release from synovial macrophages
Miller, L. E., Jüsten, H., Schcölmerich, J., & Straub, R. H. (2000) · The FASEB Journal · doi:10.1096/fj.99-1082com · Cited by 294 · see citing works
Interleukin-1: a possible role in the infertility associated with endometriosis
Fakih, H., Baggett, B., Holtz, G., Tsang, K.-Y., Lee, J. C., & Williamson, H. O. (1987) · Fertility and Sterility · doi:10.1016/s0015-0282(16)49993-0 · Cited by 285 · see citing works
Chemotactic response of nerve fiber elongation to nerve growth factor
Letourneau, P. C. (1978) · Developmental Biology · doi:10.1016/0012-1606(78)90283-x · Cited by 277 · see citing works
Basal and stimulated secretion of cytokines by peritoneal macrophages in women with endometriosis
Rana, N., Braun, D. P., House, R., Gebel, H., Rotman, C., & Dmowski, W. P. (1996) · Fertility and Sterility · doi:10.1016/s0015-0282(16)58262-4 · Cited by 264 · see citing works
It takes nerve to tell T and B cells what to do
Kin, N. W., & Sanders, V. M. (2006) · Journal of Leukocyte Biology · doi:10.1189/jlb.1105625 · Cited by 254 · see citing works
Mediator release from mast cells by nerve growth factor. Neurotrophin specificity and receptor mediation
Horigome, K., Pryor, J. C., Bullock, E. D., & Johnson, E. M. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)82415-2 · Cited by 237 · see citing works
Spontaneous Apoptosis of Endometrial Tissue is Impaired in Women with Endometriosis
Gebel, H. M., Braun, D. P., Tambur, A. R., Frame, D. G., Rana, N., & Dmowski, W. P. (1998) · Fertility and Sterility · doi:10.1016/s0015-0282(98)00073-9 · Cited by 228 · see citing works
Innervation of ectopic endometrium in a rat model of endometriosis
Berkley, K. J., Dmitrieva, N., Curtis, K. S., & Papka, R. E. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0403663101 · Cited by 227 · see citing works
Effect of nerve growth factor on the release of inflammatory mediators by mature human basophils
Bischoff, S., & Dahinden, C. A. (1992) · Blood · doi:10.1182/blood.v79.10.2662.2662 · Cited by 225 · see citing works
Classification of endometriotic implants by morphologic appearance and capacity to synthesize prostaglandin F
Vernon, M. W., Beard, J. S., Graves, K., & Wilson, E. A. (1986) · Fertility and Sterility · doi:10.1016/s0015-0282(16)49814-6 · Cited by 204 · see citing works
Cooperative regulation of nerve growth factor synthesis and secretion in fibroblasts and astrocytes by fibroblast growth factor and other cytokines
Yoshida, K., & Gage, F. H. (1992) · Brain Research · doi:10.1016/0006-8993(92)90364-f · Cited by 202 · see citing works
Endocrinology and paracrinology
Arici, A. M., Tazuke, S. I., Kliman, H. J., & Olive, D. L. (1996) · Molecular Human Reproduction · doi:10.1093/molehr/2.1.40 · Cited by 201 · see citing works
Some characteristics of histamine secretion from rat peritoneal mast cells stimulated with nerve growth factor.
Pearce, F. L., & Thompson, H. L. (1986) · The Journal of Physiology · doi:10.1113/jphysiol.1986.sp016014 · Cited by 196 · see citing works
Role of neurotrophin signalling in the differentiation of neurons from dorsal root ganglia and sympathetic ganglia
Ernsberger, U. (2009) · Cell and Tissue Research · doi:10.1007/s00441-009-0784-z · Cited by 194 · see citing works
Cutaneous hyperalgesia induced by peripheral injection of interleukin-1β in the rat
Fukuoka, H., Kawatani, M., Hisamitsu, T., & Takeshige, C. (1994) · Brain Research · doi:10.1016/0006-8993(94)90960-1 · Cited by 194 · see citing works
Endometrial Anomalies in Women with Endometriosis
Sharpe-Timms, K. L. (2001) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2001.tb03797.x · Cited by 187 · see citing works
Effect of nerve growth factor on the release of inflammatory mediators by mature human basophils
Bischoff, S., & Dahinden, C. A. (1992) · Blood · doi:10.1182/blood.v79.10.2662.bloodjournal79102662 · Cited by 187 · see citing works
The influence of nerve growth factor on the in vitro proliferative response of rat spleen lymphocytes
Thorpe, L. W., & Perez-Polo, J. R. (1987) · Journal of Neuroscience Research · doi:10.1002/jnr.490180120 · Cited by 155 · see citing works
An opposing time‐dependent immune‐modulating effect of the sympathetic nervous system conferred by altering the cytokine profile in the local lymph nodes and spleen of mice with type II collagen–induced arthritis
Härle, P., Möbius, D., Carr, D. J. J., Schölmerich, J., & Straub, R. H. (2005) · Arthritis & Rheumatism · doi:10.1002/art.20987 · Cited by 151 · see citing works
Beta 2-adrenergic mechanisms in experimental arthritis.
Levine, J. D., Coderre, T. J., Helms, C. A., & Basbaum, A. I. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.12.4553 · Cited by 145 · see citing works
Neurotrophic Factors: Important Regulators of Nociceptive Function
Bennett, D. (2001) · The Neuroscientist · doi:10.1177/107385840100700105 · Cited by 145 · see citing works
Neurite extension of chicken peripheral nervous system neurons on fibronectin: relative importance of specific adhesion sites in the central cell-binding domain and the alternatively spliced type III connecting segment.
Humphries, M. J., Akiyama, S. K., Komoriya, A., Olden, K., & Yamada, K. M. (1988) · The Journal of Cell Biology · doi:10.1083/jcb.106.4.1289 · Cited by 135 · see citing works
New considerations for the pathogenesis of endometriosis
Gazvani, R., & Templeton, A. (2002) · International Journal of Gynecology & Obstetrics · doi:10.1016/s0020-7292(01)00577-x · Cited by 127 · see citing works
Regulation of cutaneous C-fiber heat nociceptors by nerve growth factor in the developing rat
Lewin, G. R., & Mendell, L. M. (1994) · Journal of Neurophysiology · doi:10.1152/jn.1994.71.3.941 · Cited by 124 · see citing works
Endometriosis: abnormal endometrium and dysfunctional immune response
Braun, D. P., & Dmowski, W. P. (1998) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/00001703-199810000-00003 · Cited by 123 · see citing works
Elevated concentration and biologic activity of monocyte chemotactic protein-1 in the peritoneal fluid of patients with endometriosis
Daya, S., Akoum, A., Lemay, A., McColl, S. R., Turcot-Lemay, L., & Maheux, R. (1996) · Fertility and Sterility · doi:10.1016/s0015-0282(16)58381-2 · Cited by 121 · see citing works
Growth-associated protein 43–positive sensory nerve fibers accompanied by immature vessels are located in or near peritoneal endometriotic lesions
Mechsner, S., Schwarz, J., Thode, J., Loddenkemper, C., Salomon, D. S., & Ebert, A. D. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2006.12.087 · Cited by 114 · see citing works
Self-citation
Mast Cells: The Neuroimmune Connection
Williams, R. M., Bienenstock, J., & Stead, R. H. (2015) · Chemical immunology/Fortschritte der Allergielehre/Progress in allergy/Chemical immunology and allergy · doi:10.1159/000424590 · Cited by 112 · see citing works
Low density of sympathetic nerve fibres and increased density of brain derived neurotrophic factor positive cells in RA synovium
Weidler, C., Holzer, C., Harbuz, M., Hofbauer, R., Angele, P., Schölmerich, J., & Straub, R. H. (2004) · Annals of the Rheumatic Diseases · doi:10.1136/ard.2003.016154 · Cited by 103 · see citing works
Oestrogen regulates sympathetic neurite outgrowth by modulating brain derived neurotrophic factor synthesis and release by the rodent uterus
Krizsan‐Agbas, D., Pedchenko, T., Hasan, W., & Smith, P. G. (2003) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2003.03029.x · Cited by 99 · see citing works
Nerve growth factor NT-5 induce increased thermal sensitivity of cutaneous nociceptors in vitro
Rueff, A., & Mendell, L. M. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.76.5.3593 · Cited by 98 · see citing works
Tumor necrosis factor is markedly synergistic with interleukin 1 and interferon‐γ in stimulating the production of nerve growth factor in fibroblasts
Hattori, A., Iwasaki, S., Murase, K., Tsujimoto, M., Sato, M., Hayashi, K., & Kohno, M. (1994) · FEBS Letters · doi:10.1016/0014-5793(94)80132-0 · Cited by 97 · see citing works
Overexpression of nerve growth factor in peritoneal fluid from women with endometriosis may promote neurite outgrowth in endometriotic lesions
Barcena de Arellano, M. L., Arnold, J., Vercellino, F., Chiantera, V., Schneider, A., & Mechsner, S. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2010.10.023 · Cited by 89 · see citing works
Self-citation
Autoimmunity in Endometriosis: Relevance to Infertility
MATHUR, S. P. (2000) · American Journal of Reproductive Immunology · doi:10.1111/j.8755-8920.2000.440204.x · Cited by 88 · see citing works
Acute and chronic estrogen supplementation decreases uterine sympathetic innervation in ovariectomized adult virgin rats.
Zoubina, E. V., Mize, A. L., Alper, R. H., & Smith, P. G. (2001) · PubMed · doi:10.14670/hh-16.989 · Cited by 85 · see citing works
Presence of Two Signaling TGF-β Receptors in Human Pancreatic Cancer Correlates with Advanced Tumor Stage
Zhao, L., Friess, H., Graber, H. U., Guo, X., Schilling, M. K., Zimmermann, A., Korc, M., & Büchler, M. W. (1997) · Digestive Diseases and Sciences · doi:10.1023/a:1018814416903 · Cited by 77 · see citing works
Airway nociceptors activated by pro-inflammatory cytokines
Yu, J., Lin, S., Zhang, J., Otmishi, P., & Guardiola, J. (2006) · Respiratory Physiology & Neurobiology · doi:10.1016/j.resp.2006.11.005 · Cited by 75 · see citing works
A rapid method for semi-quantitative analysis of neurite outgrowth from chick DRG explants using image analysis
Bilsland, J., Rigby, M., Young, L., & Harper, S. (1999) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(99)00099-0 · Cited by 75 · see citing works
Dual Role for Noradrenergic Innervation of Lymphoid Tissue and Arthritic Joints in Adjuvant-Induced Arthritis
Lorton, D., Lubahn, C. L., Klein, N., Schaller, J. A., & Bellinger, D. L. (1999) · Brain Behavior and Immunity · doi:10.1006/brbi.1999.0564 · Cited by 69 · see citing works
Epidemiology of Endometriosis
Missmer, S. A., & Cramer, D. W. (2010) · Taylor & Francis eBooks · doi:10.4324/9780203319390_chapter_4 · Cited by 69 · see citing works
Sympathetic hyperinnervation of the uterus in the estrogen receptor α knock-out mouse
Zoubina, E. V., & Smith, P. G. (2001) · Neuroscience · doi:10.1016/s0306-4522(00)00549-2 · Cited by 66 · see citing works
Neuron‐Enriched cultures of adult rat dorsal root ganglia: Establishment, characterization, survival, and neuropeptide expression in response to trophic factors
Grothe, C., & Unsicker, K. (1987) · Journal of Neuroscience Research · doi:10.1002/jnr.490180406 · Cited by 62 · see citing works
Mast Cells: The Neuroimmune Connection (Part 1 of 2)
Williams, R. M., Bienenstock, J., & Stead, R. H. (1995) · Chemical immunology/Fortschritte der Allergielehre/Progress in allergy/Chemical immunology and allergy · doi:10.1159/000319288 · Cited by 61 · see citing works
Influence of Nerve Growth Factor in Endometriosis-Associated Symptoms
Barcena, M. L., Arnold, J., Vercellino, G. F., Chiàntera, V., Ebert, A. D., Schneider, A., & Mechsner, S. (2011) · Reproductive Sciences · doi:10.1177/1933719111410711 · Cited by 53 · see citing works
Self-citation
Immunologic Aspects of Endometriosis
Dmowski, W. P. (1987) · Contributions to gynecology and obstetrics · doi:10.1159/000414847 · Cited by 51 · see citing works
REVIEW
Fay, T. N., & Grudzinskas, J. G. (1991) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a137533 · Cited by 50 · see citing works
Axonal degeneration and regeneration in rat uterus during the estrous cycle
Zoubina, E. V., & Smith, P. G. (2000) · Autonomic Neuroscience · doi:10.1016/s1566-0702(00)00209-5 · Cited by 49 · see citing works
Substance P, obesity, and gut inflammation
Karagiannides, I., & Pothoulakis, C. (2009) · Current Opinion in Endocrinology Diabetes and Obesity · doi:10.1097/med.0b013e328321306c · Cited by 49 · see citing works
Loss of sympathetic nerve fibers in intestinal endometriosis
Ferrero, S., Haas, S., Remorgida, V., Camerini, G., Fulcheri, E., Ragni, N., Straub, R. H., & Capellino, S. (2010) · Fertility and Sterility · doi:10.1016/j.fertnstert.2010.06.069 · Cited by 46 · see citing works
Geometry of isolated sensory neurons in culture
Bray, D., Bunge, M. B., & Chapman, K. (1987) · Experimental Cell Research · doi:10.1016/0014-4827(87)90422-8 · Cited by 32 · see citing works
Autoimmune disease and innervation
Straub, R. H. (2007) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2007.04.005 · Cited by 30 · see citing works
Characterization of antibodies to synthetic nerve growth factor (NGF) and ProNGF peptides
Ebendal, T., Persson, H., Larhammar, D., Lundströmer, K., & Olson, L. (1989) · Journal of Neuroscience Research · doi:10.1002/jnr.490220302 · Cited by 29 · see citing works
Detection of Antiendometrial Antibodies in Patients With Endometriosis by Cell ELISA
Hatayama, H., Imai, K., Kanzaki, H., Higuchi, T., Fujimoto, M., & Mori, T. (1996) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.1996.tb00017.x · Cited by 20 · see citing works
Epidemiology of Endometriosis
Koninckx, P. R. (2003) · CRC Press eBooks · doi:10.1201/b14235-2 · Cited by 19 · see citing works
Anti‐Endometrial Autoantibodies in Women with a Diagnosis of Infertility
Palacio, J. R., Iborra, A., Martínez, P., Gris, J. M., & Andolz, P. (1997) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.1997.tb00283.x · Cited by 16 · see citing works
Chapter 3 Nociceptors: neurogenic inflammation
Handwerker, H. O. (2006) · Handbook of clinical neurology · doi:10.1016/s0072-9752(06)80007-2 · Cited by 11 · see citing works
Organotypic cultures of chick dorsal root ganglia in a semi-solid medium: A model for neurotoxicity testing
Mandys, V., Tureček, R., Gispen, W. H., & Bär, P. R. (1994) · Toxicology in Vitro · doi:10.1016/0887-2333(94)90211-9 · Cited by 11 · see citing works
Differential loss of sympathetic nerves and increase of substance P positive nerves in the colon in Crohn’s disease: A role for the nerve repellent factor semaphorin 3C
Grum, F., Härle, P., Bataille, F., Schölmerich, J., Schubert, T. E. O., & Straub, R. H. (2006) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2006.04.055 · Cited by 4 · see citing works

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Endometriosis: Etiology, pathobiology, and therapeutic prospects
Saunders, P. T. K., & Horne, A. W. (2021) · Cell · doi:10.1016/j.cell.2021.04.041 · Cited by 1,022 · see citing works
The sympathetic nervous response in inflammation
Pongratz, G., & Straub, R. H. (2014) · Arthritis Research & Therapy · doi:10.1186/s13075-014-0504-2 · Cited by 427 · see citing works
Pain in Endometriosis
Maddern, J., Grundy, L., Castro, J., & Brierley, S. M. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.590823 · Cited by 279 · see citing works
Endometriosis-Associated Macrophages: Origin, Phenotype, and Function
Hogg, C., Horne, A. W., & Greaves, E. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.00007 · Cited by 241 · see citing works
Pathogenesis of Endometriosis: The Origin of Pain and Subfertility
Gruber, T. M., & Mechsner, S. (2021) · Cells · doi:10.3390/cells10061381 · Cited by 202 · see citing works
Self-citation
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
Self-citation
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
Research Priorities for Endometriosis: Recommendations From a Global Consortium of Investigators in Endometriosis
Peter, A. W., Adamson, G. D., Al‐Jefout, M., Becker, C. M., D’Hooghe, T. M., Dunselman, G. A. J., Fazleabas, A. T., Giudice, L. C., Horne, A. W., Hull, M. L., et al. (2016) · Reproductive Sciences · doi:10.1177/1933719116654991 · Cited by 188 · see citing works
Macrophage and nerve interaction in endometriosis
Wu, J., Xie, H., Yao, S., & Liang, Y. (2017) · Journal of Neuroinflammation · doi:10.1186/s12974-017-0828-3 · Cited by 187 · see citing works
Autonomic nervous system and inflammation interaction in endometriosis-associated pain
Wei, Y., Liang, Y., Lin, H., Dai, Y., & Yao, S. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-01752-1 · Cited by 172 · see citing works
Defining Future Directions for Endometriosis Research: Workshop Report From the 2011 World Congress of Endometriosis in Montpellier, France
Rogers, P. A. W., D’Hooghe, T. M., Fazleabas, A., Giudice, L. C., Montgomery, G. W., Petraglia, F., & Taylor, R. N. (2013) · Reproductive Sciences · doi:10.1177/1933719113477495 · Cited by 154 · see citing works
Sensory and sympathetic nerve fibers undergo sprouting and neuroma formation in the painful arthritic joint of geriatric mice
Jiménez‐Andrade, J. M., & Mantyh, P. W. (2012) · Arthritis Research & Therapy · doi:10.1186/ar3826 · Cited by 121 · see citing works
Cellular Components Contributing to Fibrosis in Endometriosis: A Literature Review
Viganò, P., Ottolina, J., Bartiromo, L., Bonavina, G., Schimberni, M., Villanacci, R., & Candiani, M. (2019) · Journal of Minimally Invasive Gynecology · doi:10.1016/j.jmig.2019.11.011 · Cited by 109 · see citing works
Peripheral, Central, and Cross Sensitization in Endometriosis-Associated Pain and Comorbid Pain Syndromes
McNamara, H. C., Frawley, H., Donoghue, J. F., Readman, E., Healey, M., Ellett, L., Reddington, C., Hicks, L. J., Harlow, K., Rogers, P. A. W., et al. (2021) · Frontiers in Reproductive Health · doi:10.3389/frph.2021.729642 · Cited by 100 · see citing works
Cancer-associated mutations in endometriosis: shedding light on the pathogenesis and pathophysiology
Guo, S.-W. (2020) · Human Reproduction Update · doi:10.1093/humupd/dmz047 · Cited by 96 · see citing works
Estrogen and female reproductive tract innervation: Cellular and molecular mechanisms of autonomic neuroplasticity
Brauer, M. M., & Smith, P. G. (2014) · Autonomic Neuroscience · doi:10.1016/j.autneu.2014.11.009 · Cited by 92 · see citing works
Sensory Neurons, Neuroimmunity, and Pain Modulation by Sex Hormones
Lenert, M. E., Avona, A., Garner, K. M., Barron, L. R., & Burton, M. D. (2021) · Endocrinology · doi:10.1210/endocr/bqab109 · Cited by 94 · see citing works
Mechanism of pain generation for endometriosis-associated pelvic pain
Kobayashi, H., Yamada, Y., Morioka, S., Niiro, E., 重光, 愛., & Ito, F. (2013) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-013-3049-8 · Cited by 85 · see citing works
Neuropeptides Substance P and Calcitonin Gene Related Peptide Accelerate the Development and Fibrogenesis of Endometriosis
Yan, D., Liu, X., & Guo, S.-W. (2019) · Scientific Reports · doi:10.1038/s41598-019-39170-w · Cited by 82 · see citing works
Evidence of neurotrophic events due to peritoneal endometriotic lesions
Barcena de Arellano, M. L., Arnold, J., Lang, H., Vercellino, G. F., Chiantera, V., Schneider, A., & Mechsner, S. (2013) · Cytokine · doi:10.1016/j.cyto.2013.03.003 · Cited by 78 · see citing works
Self-citation
Estrogen Receptor (ER) Agonists Differentially Regulate Neuroangiogenesis in Peritoneal Endometriosis via the Repellent Factor SLIT3
Greaves, E., Collins, F., Esnal-Zufiaurre, A., Giakoumelou, S., Horne, A. W., & Saunders, P. T. K. (2014) · Endocrinology · doi:10.1210/en.2014-1086 · Cited by 77 · see citing works
A Lifelong Impact on Endometriosis: Pathophysiology and Pharmacological Treatment
Chen, L.-H., Lo, W.-C., Huang, H.-Y., & Wu, H. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24087503 · Cited by 85 · see citing works
P2X3-Containing Receptors as Targets for the Treatment of Chronic Pain
Krajewski, J. L. (2020) · Neurotherapeutics · doi:10.1007/s13311-020-00934-2 · Cited by 75 · see citing works
Endometriosis, Pain, and Related Psychological Disorders: Unveiling the Interplay among the Microbiome, Inflammation, and Oxidative Stress as a Common Thread
Cuffaro, F., Russo, E., & Amedei, A. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25126473 · Cited by 82 · see citing works
Eliapixant is a selective P2X3 receptor antagonist for the treatment of disorders associated with hypersensitive nerve fibers
Davenport, A. J., Berindan‐Neagoe, I., Bräuer, N., Koch, M., Rotgeri, A., Nagel, J., Laux‐Biehlmann, A., Machet, F., Coelho, A.-M., Boyce, S., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-99177-0 · Cited by 69 · see citing works
Linzagolix: a new GnRH-antagonist under investigation for the treatment of endometriosis and uterine myomas
Dababou, S., Garzon, S., Laganà, A. S., Ferrero, S., Evangelisti, G., Noventa, M., D’Alterio, M. N., Palomba, S., Uccella, S., Franchi, M. P., et al. (2021) · Expert Opinion on Investigational Drugs · doi:10.1080/13543784.2021.1957830 · Cited by 65 · see citing works
Neurogenic Inflammation in the Context of Endometriosis—What Do We Know?
Velho, R. V., Taube, E., Sehouli, J., & Mechsner, S. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222313102 · Cited by 62 · see citing works
Self-citation
Genome-wide association analysis of pain severity in dysmenorrhea identifies association at chromosome 1p13.2, near the nerve growth factor locus
Jones, A. V., Hockley, J. R. F., Hyde, C. L., Gorman, D. N., Sredic-Rhodes, A., Bilsland, J., McMurray, G., Furlotte, N. A., Hu, Y., Hinds, D. A., et al. (2016) · Pain · doi:10.1097/j.pain.0000000000000678 · Cited by 65 · see citing works
Relevant human tissue resources and laboratory models for use in endometriosis research
Greaves, E., Critchley, H., Horne, A. W., & Saunders, P. T. K. (2017) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1111/aogs.13119 · Cited by 62 · see citing works
Endometriosis-Related Chronic Pelvic Pain
Song, S. Y., Jung, Y. W., Shin, W., Park, M., Lee, G. W., Jeong, S., An, S., Kim, K.-M., Ko, Y. B., Lee, K. H., et al. (2023) · Biomedicines · doi:10.3390/biomedicines11102868 · Cited by 67 · see citing works
Interactions Between The Painful Disorders and The Autonomic Nervous System
Arslan, D. (2022) · Ağrı - The Journal of The Turkish Society of Algology · doi:10.14744/agri.2021.43078 · Cited by 59 · see citing works
P2X3 receptor involvement in endometriosis pain via ERK signaling pathway
Ding, S., Zhu, L., Tian, Y., Zhu, T., Huang, X., & Zhang, X. (2017) · PLoS ONE · doi:10.1371/journal.pone.0184647 · Cited by 55 · see citing works
Sensory nerve-derived neuropeptides accelerate the development and fibrogenesis of endometriosis
Liu, X., Yan, D., & Guo, S.-W. (2019) · Human Reproduction · doi:10.1093/humrep/dey392 · Cited by 51 · see citing works
The Importance of Pelvic Nerve Fibers in Endometriosis
Miller, E. J., & Fraser, I. S. (2015) · Women s Health · doi:10.2217/whe.15.47 · Cited by 52 · see citing works
Eutopic stromal cells of endometriosis promote neuroangiogenesis via exosome pathway†
Sun, H., Li, D., Yuan, M., Li, Q., Li, N., & Wang, G. (2018) · Biology of Reproduction · doi:10.1093/biolre/ioy212 · Cited by 50 · see citing works
Is primary dysmenorrhea a precursor of future endometriosis development?
Clemenza, S., Vannuccini, S., Capezzuoli, T., Meleca, C. I., Pampaloni, F., & Petraglia, F. (2021) · Gynecological Endocrinology · doi:10.1080/09513590.2021.1878134 · Cited by 50 · see citing works
Nerve fibers and endometriotic lesions: partners in crime in inflicting pains in women with endometriosis
Yan, D., Liu, X., & Guo, S. (2016) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2016.06.017 · Cited by 48 · see citing works
How to Understand the Complexity of Endometriosis-Related Pain
Chiàntera, V., Abesadze, E., & Mechsner, S. (2017) · Journal of Endometriosis and Pelvic Pain Disorders · doi:10.5301/je.5000271 · Cited by 49 · see citing works
Self-citation
Important role of collective cell migration and nerve fiber density in the development of deep nodular endometriosis
Orellana, R., García-Solares, J., Donnez, J., Kerk, O. V., Dolmans, M., & Donnez, O. (2017) · Fertility and Sterility · doi:10.1016/j.fertnstert.2017.01.005 · Cited by 45 · see citing works
Dienogest inhibits nerve growth factor expression induced by tumor necrosis factor-α or interleukin-1β
Mita, S., Shimizu, Y., Sato, A., Notsu, T., Imada, K., & Kyo, S. (2013) · Fertility and Sterility · doi:10.1016/j.fertnstert.2013.10.038 · Cited by 43 · see citing works
Neuroimmunomodulatory Alterations in Non-Lesional Peritoneum Close to Peritoneal Endometriosis
Arnold, J., Vercellino, G. F., Chiàntera, V., Schneider, A., Mechsner, S., & Barcena, M. L. (2012) · NeuroImmunoModulation · doi:10.1159/000342163 · Cited by 42 · see citing works
Self-citation
Potential role of estrogen in maintaining the imbalanced sympathetic and sensory innervation in endometriosis
Liang, Y., & Yao, S. (2016) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.01.012 · Cited by 41 · see citing works
Fractalkine/CX3CR1 Contributes to Endometriosis-Induced Neuropathic Pain and Mechanical Hypersensitivity in Rats
Liu, Z., Chen, S., Qiu, C., Sun, Y., Li, W., Jiang, J., & Zhang, J. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00495 · Cited by 38 · see citing works
Adrenergic Signaling in Immunotherapy of Cancer: Friend or Foe?
Jensen, A. W. P., Simões, A. M. C., Straten, P. T., & Olofsson, G. H. (2021) · Cancers · doi:10.3390/cancers13030394 · Cited by 35 · see citing works
Is acupuncture effective in the treatment of pain in endometriosis?
Lund, I., & Lundeberg, T. (2016) · Journal of Pain Research · doi:10.2147/jpr.s55580 · Cited by 33 · see citing works
The peritoneum—an important factor for pathogenesis and pain generation in endometriosis
Barcena, M. L., & Mechsner, S. (2014) · Journal of Molecular Medicine · doi:10.1007/s00109-014-1135-4 · Cited by 33 · see citing works
Self-citation
Perineural invasion in endometriotic lesions contributes to endometriosis-associated pain
Liang, Y., Liu, D., Yang, F., Pan, W., Zeng, F., Wu, J., Xie, H., Li, J., & Yao, S. (2018) · Journal of Pain Research · doi:10.2147/jpr.s168715 · Cited by 32 · see citing works
Purinergic Signaling in Endometriosis-Associated Pain
Trapero, C., & Martı́n-Satué, M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21228512 · Cited by 30 · see citing works
Impaired bone morphogenetic protein (BMP) signaling pathways disrupt decidualization in endometriosis
Liao, Z., Tang, S., Jiang, P., Geng, T., Cope, D. I., Dunn, T. N., Guner, J. Z., Radilla, L. A., Guan, X., & Monsivais, D. (2024) · Communications Biology · doi:10.1038/s42003-024-05898-z · Cited by 31 · see citing works
Neuroendocrine and stress-related aspects of endometriosis.
Luisi, S. V., Pizzo, A., Pinzauti, S., Zupi, E., Centini, G., Lazzeri, L., Carlo, C. D., & Petraglia, F. (2015) · PubMed · Cited by 27 · see citing works
Endometriosis and its global impact on a woman’s body
Adamyan, L. V., & Andreeva, E. N. (2022) · Russian Journal of Human Reproduction · doi:10.17116/repro20222801154 · Cited by 27 · see citing works
The role of peripheral nerve signaling in endometriosis
Godin, S. K., Wagner, J. A., Huang, P. S., & Bree, D. (2021) · FASEB BioAdvances · doi:10.1096/fba.2021-00063 · Cited by 27 · see citing works
Neuroproliferative dyspareunia in endometriosis and vestibulodynia
Mwaura, A. N., Marshall, N., Anglesio, M. S., & Yong, P. J. (2023) · Sexual Medicine Reviews · doi:10.1093/sxmrev/qead033 · Cited by 24 · see citing works
Eutopic endometrium from women with endometriosis does not exhibit neurotrophic properties
Barcena, M. L., Arnold, J., Sacher, F., Bloechle, M., Staube, M., Bartley, J., Vercellino, G. F., Chiàntera, V., Schneider, A., & Mechsner, S. (2012) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2012.04.020 · Cited by 23 · see citing works
Self-citation
Mechanisms of peripheral sensitization in endometriosis patients with peritoneal lesions and acyclical pain
Velho, R. V., Sehouli, J., & Mechsner, S. (2023) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-023-07110-9 · Cited by 23 · see citing works
Self-citation
Identification of potent pan-ephrin receptor kinase inhibitors using DNA-encoded chemistry technology
Madasu, C., Liao, Z., Parks, S. E., Sharma, K. L., Bohren, K. M., Ye, Q., Li, F., Palaniappan, M., Tan, Z., Yuan, F., et al. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2322934121 · Cited by 23 · see citing works
Nerve fiber density in deep nodular endometriotic lesions induced in a baboon experimental model
Donnez, O., Soares, M. P. M., Defrère, S., Dehoux, J., Langendonckt, A. V., Donnez, J., Dolmans, M., & Colette, S. (2013) · Fertility and Sterility · doi:10.1016/j.fertnstert.2013.06.014 · Cited by 23 · see citing works
Localization of TrkB and p75 receptors in peritoneal and deep infiltrating endometriosis: an immunohistochemical study
Dewanto, A., Dudás, J., Glueckert, R., Mechsner, S., Schrott‐Fischer, A., Wildt, L., & Seeber, B. (2016) · Reproductive Biology and Endocrinology · doi:10.1186/s12958-016-0178-5 · Cited by 22 · see citing works
Self-citation
Neuroinflammation is responsible for pain in endometriosis - targeting the JAK-STAT pathway and mast cell activation
Golinska, M. A., Wołyniak, M., Kulesza, P., & Fendler, W. M. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1621178 · Cited by 18 · see citing works
The deep infiltrating endometriosis tissue has lower T-cadherin, E-cadherin, progesterone receptor and oestrogen receptor than endometrioma tissue
Bıyık, İ., Kalkan, Ü., & Şimşek, S. (2021) · Taiwanese Journal of Obstetrics and Gynecology · doi:10.1016/j.tjog.2021.09.017 · Cited by 17 · see citing works
Non-response to first-line hormonal treatment for symptomatic endometriosis: overcoming tunnel vision. A narrative review
Cetera, G., Merli, C. E. M., Facchin, F., Vigano', P., Pesce, E., Caprara, F., & Vercellini, P. (2023) · BMC Women's Health · doi:10.1186/s12905-023-02490-1 · Cited by 17 · see citing works
Neurotrophin Expression Is Not Affected in Uteri of Women with Adenomyosis
Barcena, M. L., Wagner, M. F., Oldeweme, J., Arnold, J., Ebert, A. D., Schneider, A., & Mechsner, S. (2012) · Journal of Molecular Neuroscience · doi:10.1007/s12031-012-9757-x · Cited by 17 · see citing works
Self-citation
Nerve Fibers are Absent in Disease-Free and Eutopic Endometrium, but Present in Endometriotic (Especially Deep) Lesions
Donnez, O., Soares, M. P. M., Defrère, S., Kerk, O. V., Langendonckt, A. V., Donnez, J., Dolmans, M., & Colette, S. (2013) · Journal of Endometriosis and Pelvic Pain Disorders · doi:10.5301/je.5000155 · Cited by 17 · see citing works
Efficacy of niclosamide on the intra-abdominal inflammatory environment in endometriosis
Shi, M.-X., Sekulovski, N., Whorton, A. E., MacLean, J., Greaves, E., & Hayashi, K. (2021) · The FASEB Journal · doi:10.1096/fj.202002541rrr · Cited by 13 · see citing works
The link between immunity and hypertension in the kidney and heart
Benson, L. N., Guo, Y., Deck, K. S., Mora, C. J., Liu, Y., & Mu, S. (2023) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2023.1129384 · Cited by 17 · see citing works
The Role of Abnormal Uterine Junction Zone in the Occurrence and Development of Adenomyosis
Xie, T., Xu, X., Yang, Y. L., Wu, C., Liu, X., Zhou, L., & Song, Y. (2021) · Reproductive Sciences · doi:10.1007/s43032-021-00684-2 · Cited by 16 · see citing works
L1 Cell Adhesion Molecule as a Potential Therapeutic Target in Murine Models of Endometriosis Using a Monoclonal Antibody Approach
Silveira, C. G. T., Finas, D., Hunold, P., Köster, F., Stroschein, K., Canny, G., Moldenhauer, G., Altevogt, P., Rody, A., & Hornung, D. (2013) · PLoS ONE · doi:10.1371/journal.pone.0082512 · Cited by 16 · see citing works
Inflammation-mediated macrophage polarization induces TRPV1/TRPA1 heteromers in endometriosis.
Zhu, H., Wang, Y., He, Y., & Yu, W. (2022) · PubMed Central · Cited by 15 · see citing works
Endometriosis-Associated Pain – Do Preclinical Rodent Models Provide a Good Platform for Translation?
Greaves, E., Rosser, M., & Saunders, P. T. K. (2020) · Advances in anatomy, embryology and cell biology · doi:10.1007/978-3-030-51856-1_3 · Cited by 14 · see citing works
Peripheral and central neuroplasticity in a mouse model of endometriosis
Castro, J., Maddern, J., Erickson, A., Harrington, A. M., & Brierley, S. M. (2023) · Journal of Neurochemistry · doi:10.1111/jnc.15843 · Cited by 14 · see citing works
Managing the neuroinflammatory pain of endometriosis in light of chronic pelvic pain
Pergolizzi, J. V., LeQuang, J. A., Coluzzi, F., El-Tallawy, S. N., Magnusson, P., Ahmed, R. S., Varrassi, G., & Porpora, M. G. (2024) · Expert Opinion on Pharmacotherapy · doi:10.1080/14656566.2024.2425727 · Cited by 14 · see citing works
Utilizing AI for the Identification and Validation of Novel Therapeutic Targets and Repurposed Drugs for Endometriosis
Liu, B. H. M., Lin, Y., Long, X., Hung, S. W., Gaponova, A. V., Ren, F., Zhavoronkov, A. A., Pun, F. W., & Wang, C. C. (2024) · Advanced Science · doi:10.1002/advs.202406565 · Cited by 13 · see citing works
Research progress of acupuncture analgesia based on autonomic nerve regulation pathway
Pang, L., Chen, X., Lan, Y., Huang, Q., Yu, X., Qi, L., & Wang, Z. (2023) · Acupuncture and Herbal Medicine · doi:10.1097/hm9.0000000000000087 · Cited by 11 · see citing works
Neuroendocrine–Immune Axis in Endometriosis: A Review on How the Nervous System Goes Beyond Pain Perception
Chang, L., Shan, J., Li, D., & Wang, X. (2025) · Biomolecules · doi:10.3390/biom15111536 · Cited by 10 · see citing works
Role of neuropeptides in patients with endometriosis: a literature review
Mosleh, H., Hosseini, S., Hajizadeh, N., Majdi, L., Ajdary, M., & Mofarahe, Z. S. (2024) · Middle East Fertility Society Journal · doi:10.1186/s43043-024-00207-4 · Cited by 10 · see citing works
The Sphingosine 1-Phosphate Axis: an Emerging Therapeutic Opportunity for Endometriosis
Zhang, F., & Lu, Y. (2023) · Reproductive Sciences · doi:10.1007/s43032-023-01167-2 · Cited by 10 · see citing works
Heme metabolism and HO‐1 in the pathogenesis and potential intervention of endometriosis
Hou, D.-Y., Lu, J., Zhang, X., Abudukeyoumu, A., Li, M., Zhu, X., & Xie, F. (2024) · American Journal of Reproductive Immunology · doi:10.1111/aji.13855 · Cited by 9 · see citing works
The voltage‐gated sodium channel Na V 1 .7 underlies endometriosis‐associated chronic pelvic pain
Castro, J., Maddern, J., Chow, C. Y., Tran, P., Vetter, I., King, G. F., & Brierley, S. M. (2023) · Journal of Neurochemistry · doi:10.1111/jnc.15795 · Cited by 9 · see citing works
Pain Mechanisms in Peritoneal Diseases Might Be Partially Regulated by Estrogen
Börner, C., Scheerer, C., Buschow, R., Chiàntera, V., Sehouli, J., & Mechsner, S. (2017) · Reproductive Sciences · doi:10.1177/1933719117715126 · Cited by 9 · see citing works
Self-citation
The involvement of peritoneal GATA6+ macrophages in the pathogenesis of endometriosis
Shi, M., MacLean, J. A., & Hayashi, K. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1396000 · Cited by 7 · see citing works
A narrative review about the intricate crosstalk among endometrium, adipose tissue, and neurons in endometriosis. The multifaceted role of leptin
Neves, D., Neto, A. C., Salazar, M. J., Fernandes, A. S., Martinho, M. S. L., Charrua, A., Rodrigues, A. R., Gouveia, A., & Almeida, H. (2024) · Obesity Reviews · doi:10.1111/obr.13879 · Cited by 7 · see citing works
Influence of endometrial nerve fibers and hormones on pain in women with endometriosis
Sommar, A., Bahat, P. Y., Özaydin, I. Y., Bixo, M., Bäckström, T. C., Oral, E., & Türkmen, Ş. (2025) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2025.113950 · Cited by 7 · see citing works
Neural plasticity of the uterus: New targets for endometrial cancer?
Español, P., Luna-Guibourg, R., Moreno, C. S., Caruana, P., Altés-Arranz, A., Rodríguez, F., Roda, O. P., Sanchez, O., Llurba, E., Rovira, R., et al. (2022) · Women s Health · doi:10.1177/17455057221095537 · Cited by 7 · see citing works
Calcium‐binding protein expression in peritoneal endometriosis‐associated nerve fibres
Barcena, M. L., Münch, S., Arnold, J., Helbig, S., Schneider, A., & Mechsner, S. (2013) · European Journal of Pain · doi:10.1002/j.1532-2149.2013.00323.x · Cited by 7 · see citing works
Self-citation
The Histamine-Associated Inflammatory Landscape of Endometriosis: Molecular Profiling of HDC, HRH1-HRH4, and Cytokines Across Lesion Subtypes
Velho, R. V., Freitag, J. H., Brueckner, A. M., Thalmeier, L., Pohl, J., & Mechsner, S. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms27010212 · Cited by 7 · see citing works
Self-citation
Nerve Bundle Density and Expression of NGF and IL-1β Are Intra-Individually Heterogenous in Subtypes of Endometriosis
Sreya, M., Tucker, D. R., Yi, J., Alotaibi, F. T., Lee, A. F., Noga, H. L., & Yong, P. J. (2024) · Biomolecules · doi:10.3390/biom14050583 · Cited by 6 · see citing works
Reduced inflammatory state promotes reinnervation of endometriotic-like lesions in TNFRp55 deficient mice
Ghersa, F., Delsouc, M. B., Goyeneche, A. A., Vallcaneras, S. S., Meresman, G. F., Telleria, C. M., & Casais, M. (2019) · Molecular Human Reproduction · doi:10.1093/molehr/gaz026 · Cited by 6 · see citing works
Sensory neuron LKB1 mediates ovarian and reproductive function
Lenert, M. E., Debner, E. K., & Burton, M. D. (2024) · Scientific Reports · doi:10.1038/s41598-024-79947-2 · Cited by 5 · see citing works
Endometriosis-associated pain: mechanism, neuroimmune signature, and translational precision strategies
Omenge, H., Kempa, P. A., Jeong, J.-W., So, K. A., & Kim, T. H. (2026) · Endocrine Reviews · doi:10.1210/endrev/bnag019 · Cited by 6 · see citing works
Distribution of Nerve Fibers in Abdominal Wall Endometriosis and Their Clinical Significance
Zhang, C., Dai, Y. Q., Zhang, J., Li, X., Jia, S., Shi, J., & Leng, J. (2024) · Journal of Pain Research · doi:10.2147/jpr.s453148 · Cited by 5 · see citing works
Invasion and nerve fibers damage in endometriosis
Бурлев, В. А. (2020) · Russian Journal of Human Reproduction · doi:10.17116/repro20202603153 · Cited by 4 · see citing works
Association between KRAS and PIK3CA Mutations and Progesterone Resistance in Endometriotic Epithelial Cell Line
Kanno, K., Nakayama, K., Razia, S., Sohel, H. I., Zahan, U. F., Sonia, S. B., Yamashita, H., Ishikawa, M., Ishibashi, T., Imamura, K., et al. (2024) · Current Issues in Molecular Biology · doi:10.3390/cimb46040224 · Cited by 3 · see citing works
Endometriosis-associated pain and adhesions — new pathogenetic aspects and therapeutic approach
Yarmolinskaya, M. I., & Adamyan, L. V. (2023) · Russian Journal of Human Reproduction · doi:10.17116/repro20232902193 · Cited by 3 · see citing works
Endometriose: Pathogenese, Symptome und Diagnostik
Mechsner, S. (2015) · Springer eBooks · doi:10.1007/978-3-662-43669-1_5 · Cited by 3 · see citing works
Self-citation
The role of acupuncture in the treatment of women with pain in endometriosis: A protocol for systematic review and meta-analysis.
Qin, Y., Li, J., & Zeng, J. (2021) · PubMed Central · doi:10.1097/md.0000000000027582 · Cited by 2 · see citing works
Pain pathways and stem cells in endometriosis pathogenesis
Aydin, H., & Elbe, H. (2025) · Molecular Biology Reports · doi:10.1007/s11033-025-10973-7 · Cited by 3 · see citing works
Pathophysiological aspects of pain syndrome in endometriosis: A review
Сахаутдинова, И. В., Хамадьянова, А. У., Gimazetdinova, L. R., Bashirova, E. R., Fatkullin, B. S., & Рафитовна, Х. Р. (2022) · GYNECOLOGY · doi:10.26442/20795696.2022.1.201361 · Cited by 2 · see citing works
Endometriosis pain and acupuncture
Lund, I., & Lundeberg, T. (2015) · Acupuncture and Related Therapies · doi:10.1016/j.arthe.2015.08.003 · Cited by 2 · see citing works
Does Dysmenorrhea Affect Clinical Features and Long-Term Surgical Outcomes of Patients With Ovarian Endometriosis? A 12-Year Retrospective Observational Cohort Study
Wu, Y., Li, X., Dai, Y., Shi, J., Gu, Z., Zhang, J., Zhang, C., Yan, H., & Leng, J. (2022) · Frontiers in Medicine · doi:10.3389/fmed.2022.905688 · Cited by 2 · see citing works
Endometriosis: The Enigma That It Continues to Be
Sharma, S., & Tripathi, A. (2022) · IntechOpen eBooks · doi:10.5772/intechopen.108774 · Cited by 3 · see citing works

Neuroimmunomodulatory Alterations in Non-Lesional Peritoneum Close to Peritoneal Endometriosis
Arnold, J., Vercellino, G. F., Schneider, A., Mechsner, S., Barcena de Arellano, M. L., & CHIANTERA, V. (2012) · Archivio Istituzionale della Ricerca - Università degli Studi del Molise
Self-citation
The role of the sympathetic and sensory nervous system in peritoneal endometriotic lesions
Arnold, J., de Arellano, M. B., Rüster, C., Schneider, A., & Mechsner, S. (2011) · Geburtshilfe und Frauenheilkunde · doi:10.1055/s-0031-1292700
Self-citation
Nerve fibres in peritoneal endometriosis
Tokushige, N., Markham, R., Russell, P., & Fraser, I. S. (2006) · Human Reproduction · doi:10.1093/humrep/del260 · Cited by 299 · see citing works
IS: Nerve fibres in peritoneal endometriosis
Tokushige, N., Markham, R., Russell, P., & Fraser, I. S. (2015)
The role of estrogen and ER α/β in the sensory and sympathetic nerve fibre imbalance in peritoneal endometriotic lesions
Arnold, J., Mechsner, S., Schneider, A., & de Arellano, M. L. B. (2013) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2013.01.031
Self-citation

Authors: Arnold, J., Barcena de Arellano, M. L., Rüster, C., Vercellino, G. F., Chiantera, V., Schneider, A., & Mechsner, S.
Affiliations: Stiftung Charité (DE)
Corresponding author: Mechsner, Sylvia
ORCID: Schneider, Achim
Mechsner, Sylvia
Venue: Brain, Behavior, and Immunity
Publisher: Elsevier BV
Published: 2012-01
Volume: 26
Issue: 1
Pages: 132-141
ISSN: 0889-1591 (ISSN-L)
DOI: 10.1016/j.bbi.2011.08.004
OpenAlex: W2057816981
Cited by: 132
References: 83
Citations by year: 2026: 6 · 2025: 8 · 2024: 17 · 2023: 14 · 2022: 8 · 2021: 19 · 2020: 8 · 2019: 4 · 2018: 6 · 2017: 6 · 2016: 9 · 2015: 9 · 2014: 5 · 2013: 9 · 2012: 4
FWCI: 6.44
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Brain Behavior and Immunity (publishedVersion)
PubMed (publishedVersion)
Archivio Istituzionale della Ricerca - Università degli Studi del Molise (submittedVersion)
Nova Science Publishers (Nova Science Publishers, Inc.) (submittedVersion)
Topics: Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
Health Sciences › Medicine › Physiology › Pain Mechanisms and Treatments
Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
Keywords: peritoneal endometriosis, endometriosis-associated pain, sensory nerve fibers, sympathetic nerve fibers, substance P, tyrosine hydroxylase, PGP 9.5, nerve growth factor, IL-1β, peritoneal fluid, dorsal root ganglia, sympathetic ganglia, neurite outgrowth, immune cell infiltration, inflammation
MeSH terms: Adult, Ascitic Fluid, Endometriosis, Female, Ganglia, Spinal, Ganglia, Sympathetic, Humans, Immunity, Cellular, Immunohistochemistry, Middle Aged, Nerve Fibers, Nerve Growth Factors, Laparoscopy, Sensory Receptor Cells, Substance P, Sympathetic Nervous System, Tyrosine 3-Monooxygenase, Stromal Cells, GAP-43 Protein, Ubiquitin Thiolesterase, Cell Proliferation, Interleukin-1beta, Young Adult

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Imbalance between sympathetic and sensory innervation in peritoneal endometriosis

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