Different types of small nerve fibers in eutopic endometrium and myometrium in women with endometriosis
Open accessAbstract
Objective To investigate types of nerve fibers in endometrium and myometrium in women with endometriosis. Design Laboratory study using human tissue. Setting University-based laboratory. Patient(s) Women with and without endometriosis undergoing hysterectomy. Intervention(s) Histologic sections of contiguous endometrial and myometrial tissues were prepared from hysterectomies performed on women with and without endometriosis. Main outcome measure(s) Types and density of nerve fibers in endometrium and myometrium in women with and without endometriosis were determined using a series of specific markers for neuronal structure and function: PGP9.5, NF, SP, CGRP, TH, VAChT, VIP, and NPY. Result(s) Nerve fibers stained with PGP9.5 and NF in endometrium and myometrium were significantly increased in women with endometriosis compared with women without endometriosis. Nerve fibers in the functional layer of endometrium in women with endometriosis were likely to be sensory C, a mixture of sensory A delta, sensory C, and adrenergic fibers in the basal layer of the endometrium, a mixture of sensory A delta, sensory C, adrenergic and cholinergic fibers in the myometrium. Conclusion(s) Increased nerve fiber density in endometrium and myometrium, and sensory C fibers and adrenergic nerve fibers in the endometrium in women with endometriosis may play an important role in the mechanisms of pain generation in this condition.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Peripheral factors associated with painful endometriosis, such as increased eutopic uterine innervation and high peritoneal fluid concentrations of prostaglandins and other pro-inflammatory agents, are also found in women without endometriosis.
“Peripheral factors associated with painful endometriosis are found in women without endometriosis, such as increased eutopic uterine innervation”
From Chronic pelvic pain and endometriosis: translational evidence of the relationship and implications (2011) · cites this paper as Tokushige et al., 2007
The Results report no nerve fibers in the functional endometrium of women without endometriosis. Myometrial fibers were present in both groups, but their density was much higher in women with endometriosis. Thus, the paper does not find the cited increase in eutopic uterine innervation in women without endometriosis. (LLM, conf=0.88)
Checked by a reasoning model — may be wrong.
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
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
BCL-2 GENE FAMILY IN THE NERVOUS SYSTEM
Merry, D. E., & Korsmeyer, S. J. (1997) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.20.1.245 · Cited by 594 · see citing works
Singer, C. A., Figueroa, X. A., Batchelor, R. H., & Dorsa, D. M. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-07-02455.1999 · Cited by 578 · see citing works
Sohrabji, F., Miranda, R. C., & Toran‐Allerand, C. D. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.24.11110 · Cited by 560 · see citing works
Mechanisms of Pain in Arthritis
Schaible, H., Ebersberger, A., & von Banchet, G. S. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb04234.x · Cited by 515 · see citing works
Singh, M., Meyer, E. M., & Simpkins, J. W. (1995) · Endocrinology · doi:10.1210/endo.136.5.7720680 · Cited by 425 · see citing works
Nervous control of the urogenital system
Maggi, C. A. (1993) · Harwood Academic Publishers eBooks · Cited by 368 · see citing works
Nilsen, J., & Brinton, R. D. (2002) · Endocrinology · doi:10.1210/endo.143.1.8582 · Cited by 331 · see citing works
Calcitonin gene-related peptide is a potent inhibitor of substance P degradation
Grevès, P. L., Nyberg, F., Terenius, L. Y., & Hökfelt, T. G. M. (1985) · European Journal of Pharmacology · doi:10.1016/0014-2999(85)90706-x · Cited by 322 · see citing works
Weihe, E., Tao-Cheng, J.-H., Schäfer, M., Erickson, J. D., & Eiden, L. E. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.8.3547 · Cited by 301 · 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
Self-citationNeurobiology of substance P and the NK1 receptor.
Mantyh, P. W. (2002) · PubMed · Cited by 284 · see citing works
Simpkins, J. W., Green, P. S., Gridley, K. E., Singh, M., de Fiebre, N. C., & Rajakumar, G. (1997) · The American Journal of Medicine · doi:10.1016/s0002-9343(97)00260-x · Cited by 270 · see citing works
Tokushige, N., Markham, R., Russell, P., & Fraser, I. S. (2006) · Human Reproduction · doi:10.1093/humrep/dei368 · Cited by 236 · see citing works
Self-citationInnervation 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
Maina, F., Hilton, M., Ponzetto, C., Davies, A. M., & Klein, R. (1997) · Genes & Development · doi:10.1101/gad.11.24.3341 · Cited by 227 · see citing works
Neurofilaments: structure, metabolism and implications in disease.
Schlaepfer, W. W. (1987) · PubMed · Cited by 200 · 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
Gibbs, R. B. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01880-6 · Cited by 186 · see citing works
Jones, D. M., Tucker, B. A., Rahimtula, M., & Mearow, K. M. (2003) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2003.01925.x · Cited by 176 · see citing works
Heat Shock Protein 27: Developmental Regulation and Expression after Peripheral Nerve Injury
Costigan, M., Mannion, R., Kendall, G. S., Lewis, S. E., Campagna, J. A., Coggeshall, R. E., Middleton, J., Tate, S., & Woolf, C. J. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-15-05891.1998 · Cited by 176 · see citing works
Angiongenesis: a new theory for endometriosis
Healy, D. (1998) · Human Reproduction Update · doi:10.1093/humupd/4.5.736 · Cited by 173 · see citing works
Schlaepfer, W. W. (1987) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-198703000-00001 · Cited by 170 · see citing works
Cardona‐Gómez, G. P., Méndez, P., DonCarlos, L. L., Azcoitia, Í., & García‐Segura, L. M. (2001) · Brain Research Reviews · doi:10.1016/s0165-0173(01)00137-0 · Cited by 166 · see citing works
A Role for HSP27 in Sensory Neuron Survival
Lewis, S. E., Mannion, R., White, F. A., Coggeshall, R. E., Beggs, S., Costigan, M., Martin, J. W., DILLMANN, W. H., & Woolf, C. J. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-20-08945.1999 · Cited by 164 · see citing works
Sensory and autonomic innervation of non-hairy and hairy human skin
Bj�rklund, H., Dalsgaard, C. ‐., Jonsson, C.-E., & Hermansson, A. (1986) · Cell and Tissue Research · doi:10.1007/bf00221851 · Cited by 157 · see citing works
Ghahary, A., & Murphy, L. J. (1989) · Endocrinology · doi:10.1210/endo-125-2-597 · Cited by 134 · see citing works
Angiogenesis occurs by vessel elongation in proliferative phase human endometrium
Gambino, L. S. (2002) · Human Reproduction · doi:10.1093/humrep/17.5.1199 · Cited by 130 · see citing works
Protein gene product 9.5 (PGP 9.5)
Lundberg, L. M., Alm, P., Wharton, J., & Polak, J. M. (1988) · Histochemistry and Cell Biology · doi:10.1007/bf00495700 · Cited by 128 · see citing works
Wilson, M. E., Dubal, D. B., & Wise, P. M. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02479-3 · Cited by 124 · see citing works
Khan, K. N., Masuzaki, H., Fujishita, A., Kitajima, M., Sekine, I., Matsuyama, T., & Ishimaru, T. (2005) · Human Reproduction · doi:10.1093/humrep/deh897 · Cited by 123 · see citing works
Estrogen receptor-dependent regulation of sensory neuron survival in developing dorsal root ganglion
Patrone, C., Andersson, S., Korhonen, L., & Lindholm, D. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.19.10905 · Cited by 120 · see citing works
Autonomic innervation of the rat vagina, cervix, and uterus and its cyclic variation
Adham, N., & Schenk, E. A. (1969) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(16)34239-9 · Cited by 113 · see citing works
Kimpinski, K., & Mearow, K. M. (2001) · Journal of Neuroscience Research · doi:10.1002/jnr.1043 · Cited by 110 · see citing works
Pharmacology of noradrenaline and neuropeptide tyrosine (NPY)‐mediated sympathetic cotransmission
Lundberg, J. O., Franco‐Cereceda, A., Hemsén, A., Js, L., & Pernow, J. (1990) · Fundamental and Clinical Pharmacology · doi:10.1111/j.1472-8206.1990.tb00692.x · Cited by 103 · see citing works
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
Vasoactive intestinal peptide (VIP) is a modulator of joint pain in a rat model of osteoarthritis
McDougall, J. J., Watkins, L., & Li, Z. (2006) · Pain · doi:10.1016/j.pain.2006.02.015 · Cited by 89 · see citing works
Production of Hyperalgesic Prostaglandins by Sympathetic Postganglionic Neurons
Gonzales, R., Goldyne, M. E., Taiwo, Y. O., & Levine, J. D. (1989) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1989.tb08557.x · Cited by 89 · see citing works
Fernandez, A. M., de la Vega, A. G., Planas, B., & Torres‐Alemán, I. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00623.x · Cited by 86 · see citing works
Differences in uterine innervation at hysterectomy
Quinn, M. J., & Kirk, N. (2002) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2002.130007 · Cited by 86 · see citing works
Calcitonin gene-related peptide inhibits spontaneous contractions in human uterus and fallopian tube
Samuelson, U., Dalsgaard, C., Lundberg, J. M., & Hökfelt, T. G. M. (1985) · Neuroscience Letters · doi:10.1016/0304-3940(85)90359-3 · Cited by 83 · see citing works
Tamburro, S., Canis, M., Albuisson, E., Dechelotte, P., Darcha, C., & Mage, G. (2003) · Fertility and Sterility · doi:10.1016/s0015-0282(03)01182-8 · Cited by 79 · see citing works
Schuelert, N., & McDougall, J. J. (2006) · Osteoarthritis and Cartilage · doi:10.1016/j.joca.2006.04.016 · Cited by 78 · see citing works
Uterine innervation after hysterectomy for chronic pelvic pain with, and without, endometriosis
Atwal, G., du Plessis, D., Armstrong, G., Slade, R., & Quinn, M. (2005) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2005.05.035 · Cited by 78 · see citing works
Bcl-2 influences axonal growth rate in embryonic sensory neurons
Hilton, M., Middleton, G., & Davies, A. M. (1997) · Current Biology · doi:10.1016/s0960-9822(06)00339-3 · Cited by 75 · see citing works
Peripheral hyperalgesia in experimental neuropathy: exacerbation by neuropeptide Y
Tracey, D. J., Romm, M. A., & Yao, N. N. L. (1995) · Brain Research · doi:10.1016/0006-8993(94)01265-j · Cited by 73 · see citing works
Nerve Fibers and Histopathology of Endometriosis-Harboring Peritoneum
Tulandi, T., Felemban, A., & Fong Chen, M. (2001) · The Journal of the American Association of Gynecologic Laparoscopists · doi:10.1016/s1074-3804(05)60556-7 · Cited by 60 · see citing works
Lynch, E. M., Wharton, J., Bryant, M. G., Bloom, S. R., Polak, J. M., & Elder, M. G. (1980) · Histochemistry · doi:10.1007/bf00493234 · Cited by 54 · see citing works
NPY-like immunoreactivity in sensory nerve fibers in rat sciatic neuroma
́n, J. F., Risling, M., Theodorsson, E., & Fried, K. (1992) · Brain Research · doi:10.1016/0006-8993(92)90547-m · Cited by 52 · see citing works
Intrathecal neuropeptide Y exacerbates nerve injury-induced mechanical hyperalgesia
White, D. M. (1997) · Brain Research · doi:10.1016/s0006-8993(96)01340-6 · Cited by 43 · see citing works
Peptidergic innervation of the human and guinea pig uterus
Heinrich, D., Reinecke, M., & Forssmann, W. (1986) · Archives of Gynecology and Obstetrics · doi:10.1007/bf02133783 · Cited by 40 · see citing works
Tang, P., Gannon, M. J., Andrew, A. C., & Miller, D. (1995) · European Journal of Endocrinology · doi:10.1530/eje.0.1330598 · Cited by 35 · see citing works
Banik, R. K., Sato, J., Yajima, H., & Mizumura, K. (2001) · Neuroscience Letters · doi:10.1016/s0304-3940(00)01770-5 · Cited by 33 · see citing works
Stjernquist, M., & Owman, C. (1987) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1987.tb08275.x · Cited by 32 · see citing works
Mini-review: estrogen action in the uterus and insulin-like growth factor-I.
Moyano, P., & Rotwein, P. (2004) · Growth Hormone & IGF Research · doi:10.1016/j.ghir.2004.09.001 · Cited by 29 · see citing works
Expression of vasoactive intestinal peptide (VIP) receptors in human uterus
Bajo, A. M., Juarranz, Y., Valenzuela, P. L., Martı́nez, P., Prieto, J. C., & Guijarro, L. G. (2000) · Peptides · doi:10.1016/s0196-9781(00)00282-5 · Cited by 22 · see citing works
Houdeau, É., Boyer, P., Rousseau, A., & Rousseau, J.-P. (1997) · Cell and Tissue Research · doi:10.1007/s004410050814 · Cited by 21 · see citing works
Fried, G. M., Hökfelt, T. G. M., Lundberg, J. M., Terenius, L. Y., & Hamberger, L. (1986) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a136424 · Cited by 19 · see citing works
Rodríguez, R., Pozuelo, J. M., Martín, R., Arriazu, R., & Santamarı́a, L. (2005) · Journal of Andrology · doi:10.1002/j.1939-4640.2005.tb01086.x · Cited by 17 · see citing works
Reinecke, M. (1987) · Neuroscience Letters · doi:10.1016/0304-3940(87)90248-5 · Cited by 16 · see citing works
Uterine nerve fibre proliferation in advanced endometriosis
Quinn, M. J., & Armstrong, G. R. (2004) · Journal of Obstetrics and Gynaecology · doi:10.1080/01443610400019203 · Cited by 16 · see citing works
Leroy, M., Tanguy, G., Vial, M., Rostène, W. H., Malassiné, A., & Ferré, F. (1991) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.1991.tb01433.x · Cited by 16 · see citing works
Pharmacological effects and metabolism of neurotensin and bradykinin in the isolated rat uterus
Lebrun, I., de Camargo, A. C. M., & Corrêa, F. M. D. A. (1988) · European Journal of Pharmacology · doi:10.1016/0014-2999(88)90568-7 · Cited by 11 · see citing works
Proliferation of myometrial nerves in a patient with severe dysmenorrhea.
Ej, L., Jaffe, M., Hj, R., & McDuff, H. C. (1985) · PubMed · Cited by 6 · see citing works
The adrenergic and cholinergic innervation of the thyroid chicken gland.
Baryła, J., Greniuk, G., & Łakomy, M. (2003) · PubMed · Cited by 5 · see citing works
Letinić, K., & Kostović, I. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970804)384:3 · Cited by 3 · see citing works
Flagged first, then by citations
1 of the 67 references couldn’t be matched to a known paper.
Research works printed but not linked: 1
- Plumier JC, Hopkins DA, Robertson HA, Currie RW. Constitutive ex- pression of the 27-kDa heat shock protein (Hsp27) in sensory and motor neurons of the rat nervous system. J Comp Neurol 1997;384:409-28.
Cited by
Sorted by citations
Endometriosis and infertility: pathophysiology and management
de Ziegler, D., Borghese, B., & Chapron, C. (2010) · The Lancet · doi:10.1016/s0140-6736(10)60490-4 · Cited by 836 · see citing works
Chronic pelvic pain and endometriosis: translational evidence of the relationship and implications
Stratton, P., & Berkley, K. J. (2011) · Human Reproduction Update · doi:10.1093/humupd/dmq050 · Cited by 442 · see citing works
Calcitonin gene-related peptide and pain: a systematic review
Schou, W. S., Ashina, S., Amin, F. M., Goadsby, P. J., & Ashina, M. (2017) · The Journal of Headache and Pain · doi:10.1186/s10194-017-0741-2 · Cited by 254 · see citing works
Rich innervation of deep infiltrating endometriosis
Wang, G., Tokushige, N., Markham, R., & Fraser, I. S. (2008) · Human Reproduction · doi:10.1093/humrep/den464 · Cited by 232 · see citing works
Self-citationRahmioglu, N., Fassbender, A., Vitonis, A. F., Tworoger, S. S., Hummelshoj, L., D'Hooghe, T. M., Adamson, G. D., Giudice, L. C., Becker, C. M., Zondervan, K. T., et al. (2014) · Fertility and Sterility · doi:10.1016/j.fertnstert.2014.07.1208 · Cited by 227 · see citing works
Self-citationEndometriosis: The Role of Neuroangiogenesis
Asante, A., & Taylor, R. N. (2011) · Annual Review of Physiology · doi:10.1146/annurev-physiol-012110-142158 · Cited by 223 · see citing works
Endometriosis and Mechanisms of Pelvic Pain
Howard, F. M. (2009) · Journal of Minimally Invasive Gynecology · doi:10.1016/j.jmig.2009.06.017 · Cited by 218 · 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
Endometrial biomarkers for the non-invasive diagnosis of endometriosis
Gupta, D., Hull, M. L., Fraser, I. S., Miller, L., Bossuyt, P. M., JOHNSON, N. P., & Nisenblat, V. (2016) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd012165 · Cited by 174 · see citing works
Self-citationFassbender, A., Rahmioglu, N., Vitonis, A. F., Viganò, P., Giudice, L. C., D’Hooghe, T. M., Hummelshoj, L., Adamson, G. D., Becker, C. M., Missmer, S. A., et al. (2014) · Fertility and Sterility · doi:10.1016/j.fertnstert.2014.07.1209 · Cited by 162 · see citing works
Self-citationAl-Jefout, M., Dezarnaulds, G., Cooper, M., Tokushige, N., Luscombe, G. M., Markham, R., & Fraser, I. S. (2009) · Human Reproduction · doi:10.1093/humrep/dep275 · Cited by 151 · see citing works
Self-citationFassbender, A., Vodolazkaia, A., Saunders, P., Lebovic, D., Waelkens, E., De Moor, B., & D'Hooghe, T. (2013) · Fertility and Sterility · doi:10.1016/j.fertnstert.2013.01.097 · Cited by 150 · see citing works
Molecular Evidence for Differences in Endometrium in Severe Versus Mild Endometriosis
Aghajanova, L., & Giudice, L. C. (2011) · Reproductive Sciences · doi:10.1177/1933719110386241 · Cited by 146 · see citing works
Bokor, A., Kyama, C. M., Vercruysse, L., Fassbender, A., Gevaert, O., Vodolazkaia, A., De Moor, B., Fulop, V., & D'Hooghe, T. (2009) · Human Reproduction · doi:10.1093/humrep/dep283 · Cited by 128 · see citing works
The eutopic endometrium in endometriosis: are the changes of clinical significance?
Brosens, I. A., Brosens, J. J., & Benagiano, G. (2012) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2012.01.022 · Cited by 124 · see citing works
Li, T. X., Mamillapalli, R., Ding, S., Chang, H., Liu, Z.-W., Gao, X., & Taylor, H. S. (2018) · Biology of Reproduction · doi:10.1093/biolre/ioy035 · Cited by 116 · see citing works
de Ziegler, D., Gayet, V., Aubriot, F. X., Fauque, P., Streuli, I., Wolf, J. P., de Mouzon, J., & Chapron, C. (2010) · Fertility and Sterility · doi:10.1016/j.fertnstert.2010.05.056 · Cited by 112 · see citing works
Lu, Y., Nie, J., Liu, X., Zheng, Y., & Guo, S. (2010) · Human Reproduction · doi:10.1093/humrep/dep472 · Cited by 111 · see citing works
Endometrial nerve fibers in women with endometriosis, adenomyosis, and uterine fibroids
Zhang, X., Lu, B., Huang, X., Xu, H., Zhou, C., & Lin, J. (2009) · Fertility and Sterility · doi:10.1016/j.fertnstert.2009.05.016 · Cited by 110 · see citing works
Mechsner, S., Kaiser, A., Kopf, A., Gericke, C., Ebert, A., & Bartley, J. (2009) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.09.006 · Cited by 107 · see citing works
Innervation of endometrium and myometrium in women with painful adenomyosis and uterine fibroids
Zhang, X., Lu, B., Huang, X., Xu, H., Zhou, C., & Lin, J. (2010) · Fertility and Sterility · doi:10.1016/j.fertnstert.2009.03.026 · Cited by 100 · see citing works
Aghajanova, L., Tatsumi, K., Horcajadas, J. A., Zamah, A. M., Esteban, F. J., Herndon, C. N., Conti, M., & Giudice, L. C. (2010) · Biology of Reproduction · doi:10.1095/biolreprod.110.086181 · Cited by 99 · see citing works
He, W., Liu, X., Zhang, Y., & Guo, S. (2010) · Reproductive Sciences · doi:10.1177/1933719110381927 · Cited by 96 · see citing works
Brauer, M. M., & Smith, P. G. (2014) · Autonomic Neuroscience · doi:10.1016/j.autneu.2014.11.009 · Cited by 92 · see citing works
Tokushige, N., Markham, R., Russell, P., & Fraser, I. S. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.08.074 · Cited by 85 · see citing works
Self-citationHyperinnervation in Intestinal Deep Infiltrating Endometriosis
Wang, G., Tokushige, N., Russell, P., Dubinovsky, S., Markham, R., & Fraser, I. S. (2009) · Journal of Minimally Invasive Gynecology · doi:10.1016/j.jmig.2009.07.012 · Cited by 85 · see citing works
Self-citationProteomic identification of neurotrophins in the eutopic endometrium of women with endometriosis
Browne, A. S., Yu, J., Huang, R.-P., Francisco, A. M. C., Sidell, N., & Taylor, R. N. (2012) · Fertility and Sterility · doi:10.1016/j.fertnstert.2012.05.027 · Cited by 78 · see citing works
Treatment strategies for endometriosis
Rodgers, A. K., & Falcone, T. (2008) · Expert Opinion on Pharmacotherapy · doi:10.1517/14656566.9.2.243 · Cited by 72 · see citing works
The Endometrium in Adenomyosis
Benagiano, G., & Brosens, I. A. (2012) · Women s Health · doi:10.2217/whe.12.8 · Cited by 73 · see citing works
Al-Jefout, M., Andreadis, N., Tokushige, N., Markham, R., & Fraser, I. (2007) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2007.04.032 · Cited by 68 · see citing works
Self-citationOptimal uterine anatomy and physiology necessary for normal implantation and placentation
de Ziegler, D., Pirtea, P., Galliano, D., Cicinelli, E., & Meldrum, D. R. (2016) · Fertility and Sterility · doi:10.1016/j.fertnstert.2016.02.023 · Cited by 67 · see citing works
Angiogenesis lymphangiogenesis and neurogenesis in endometriosis
Hey‐Cunningham, A. J. (2013) · Frontiers in Bioscience-Elite · doi:10.2741/e682 · Cited by 68 · see citing works
Endometriosis-associated nerve fibers and pain.
MEDINA, M. G., & LEBOVIC, D. I. (2009) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1080/00016340903176826 · Cited by 63 · see citing works
Nonsurgical mouse model of endometriosis-associated pain that responds to clinically active drugs
Fattori, V., Franklin, N. S., González‐Cano, R., Peterse, D., Ghalali, A., Madrian, E., Verri, W. A., Jr., Andrews, N. C., Woolf, C. J., & Rogers, M. S. (2020) · Pain · doi:10.1097/j.pain.0000000000001832 · Cited by 58 · see citing works
Delanerolle, G., Ramakrishnan, R., Hapangama, D. K., Zeng, Y., Shetty, A., Elneil, S., Chong, S., Hirsch, M., Oyewole, M., Phiri, P., et al. (2021) · Women s Health · doi:10.1177/17455065211019717 · Cited by 61 · see citing works
Stress, pain, anxiety, and depression in endometriosis–Targeting glial activation and inflammation
Mokhtari, T., Irandoost, E., & Sheikhbahaei, F. (2024) · International Immunopharmacology · doi:10.1016/j.intimp.2024.111942 · Cited by 56 · see citing works
Fattori, V., Zaninelli, T. H., Rasquel-Oliveira, F. S., Heintz, O. K., Jain, A., Sun, L., Seshan, M. L., Peterse, D., Lindholm, A. E., Anchan, R. M., et al. (2024) · Science Translational Medicine · doi:10.1126/scitranslmed.adk8230 · Cited by 64 · see citing works
Bentamapimod (JNK Inhibitor AS602801) Induces Regression of Endometriotic Lesions in Animal Models
Palmer, S. S., Altan, M., Denis, D., Tos, E. G., Gotteland, J., Osteen, K. G., Bruner‐Tran, K. L., & Nataraja, S. G. (2015) · Reproductive Sciences · doi:10.1177/1933719115600553 · Cited by 54 · see citing works
Role of Brain-Derived Neurotrophic Factor in Endometriosis Pain
Ding, S., Zhu, T., Tian, Y., Xu, P., Chen, Z., Huang, X., & Zhang, X. (2017) · Reproductive Sciences · doi:10.1177/1933719117732161 · Cited by 54 · see citing works
Bashir, S. T., Redden, C. R., Raj, K., Arcanjo, R. B., Stasiak, S., Li, Q., Steelman, A. J., & Nowak, R. A. (2023) · Journal of Neuroinflammation · doi:10.1186/s12974-023-02713-0 · Cited by 56 · 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
Self-citationYan, 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
Infertility workup: identifying endometriosis
Pirtea, P., Vulliémoz, N. R., de Ziegler, D., & Ayoubi, J. M. (2022) · Fertility and Sterility · doi:10.1016/j.fertnstert.2022.03.015 · Cited by 46 · see citing works
Tarjanne, S., Ng, C. H. M., Manconi, F., Arola, J. T., Mentula, M. J., Maneck, B., Fraser, I. S., & Heikinheimo, O. (2015) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1111/aogs.12652 · Cited by 43 · see citing works
Self-citationPullen, N., Birch, C. L., Douglas, G. J., Hussain, Q., Pruimboom-Brees, I., & Walley, R. J. (2011) · Human Reproduction Update · doi:10.1093/humupd/dmr030 · Cited by 42 · see citing works
Expression of neuronal markers in the endometrium of women with and those without endometriosis
Newman, T. A., Bailey, J. L., Stocker, L. J., Woo, Y. L., Macklon, N., & Cheong, Y. C. (2013) · Human Reproduction · doi:10.1093/humrep/det274 · Cited by 42 · see citing works
Rocha, A. L., Vieira, E. L., Ferreira, M. C., Maia, L. M., Teixeira, A. L., & Reis, F. M. (2017) · Biomarkers in Medicine · doi:10.2217/bmm-2016-0327 · Cited by 41 · see citing works
Liu, J., Liu, X., Duan, K., Zhang, Y., & Guo, S. (2012) · Reproductive Sciences · doi:10.1177/1933719112443876 · Cited by 39 · see citing works
Taylor, H. S., Dun, E. C., & Chwalisz, K. (2019) · Pain Management · doi:10.2217/pmt-2019-0010 · Cited by 38 · see citing works
Increased expression of neurogenic factors in uterine fibroids
Luddi, A., Marrocco, C., Governini, L., Semplici, B., Pavone, V., Capaldo, A., Tosti, C., Greco, S., Luisi, S. V., Ciarmela, P., et al. (2019) · Human Reproduction · doi:10.1093/humrep/dez182 · Cited by 37 · see citing works
Optimal management of chronic cyclical pelvic pain: an evidence-based and pragmatic approach
Abbott, J. (2010) · International Journal of Women s Health · doi:10.2147/ijwh.s7991 · Cited by 38 · see citing works
Mysteries of endometriosis pain: Chien‐Tien Hsu Memorial Lecture 2009
Fraser, I. S. (2010) · Journal of obstetrics and gynaecology research · doi:10.1111/j.1447-0756.2010.01181.x · Cited by 36 · see citing works
Self-citationNovel Drug Targets with Traditional Herbal Medicines for Overcoming Endometriosis
İlhan, M., Dereli, F. T. G., & Akkol, E. K. (2018) · Current Drug Delivery · doi:10.2174/1567201816666181227112421 · Cited by 36 · see citing works
Diagnosis of endometrial nerve fibers in women with endometriosis
Aghaey Meibody, F., Mehdizadeh Kashi, A., Zare Mirzaie, A., Ghajarie Bani Amam, M., Shariati Behbahani, A., Zolali, B., & Najafi, L. (2011) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-010-1806-5 · Cited by 35 · see citing works
Ellett, L., Readman, E., Newman, M. R., McIlwaine, K., Villegas, R., Jagasia, N., & Maher, P. J. (2015) · Human Reproduction · doi:10.1093/humrep/dev259 · Cited by 33 · see citing works
Neuroendocrine cells in eutopic endometrium of women with endometriosis
Wang, G., Tokushige, N., Russell, P., Dubinovsky, S., Markham, R., & Fraser, I. S. (2009) · Human Reproduction · doi:10.1093/humrep/dep379 · Cited by 29 · see citing works
Self-citationGuo, S., Habiba, M. A., & Benagiano, G. (2023) · Biomolecules · doi:10.3390/biom13020336 · Cited by 29 · see citing works
Nerve fibers in uterosacral ligaments of women with deep infiltrating endometriosis
Kelm, A., Lancellotti, C. L. P., Donadio, N., Auge, A. P. F., Lima, S. M. R. R., Aoki, T., & Ribeiro, P. A. (2008) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2008.08.004 · Cited by 28 · 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
Pain and endometriosis: Etiology, impact, and therapeutics
Taylor, R. N., Hummelshøj, L., Stratton, P., & Vercellini, P. (2012) · Middle East Fertility Society Journal · doi:10.1016/j.mefs.2012.09.002 · Cited by 27 · see citing works
Recent Advances in Gene Therapy of Endometriosis
Shubina, A., Egorova, A., Баранов, В. С., & Kiselev, A. (2014) · Recent Patents on DNA & Gene Sequences · doi:10.2174/18722156113079990021 · Cited by 28 · see citing works
Endometriosis and ovulatory menstruation: beyond the Sampson principle
Bulun, S. E. (2025) · Journal of Clinical Investigation · doi:10.1172/jci188787 · Cited by 28 · see citing works
Anatomic and functional mapping of human uterine innervation
Pinsard, M., Mouchet, N., Dion, L., Bessède, T., Bertrand, M. M., Daraï, É., Bellaud, P., Loget, P., Mazaud‐Guittot, S., Morandi, X., et al. (2022) · Fertility and Sterility · doi:10.1016/j.fertnstert.2022.02.013 · Cited by 26 · see citing works
Effect of siRNA Against ß-NGF on Nerve Fibers of a Rat Model With Endometriosis
Chen, Y., Dong, L., Zhang, Z., Takushige, N., Kong, B., & Wang, G.-Y. (2013) · Reproductive Sciences · doi:10.1177/1933719113497279 · Cited by 26 · see citing works
Emerging drugs for endometriosis
Guo, S. (2008) · Expert Opinion on Emerging Drugs · doi:10.1517/14728210802548360 · Cited by 25 · see citing works
The Autonomic Innervation and Uterine Telocyte Interplay in Leiomyoma Formation
Aleksandrovych, V., Kurnik‐Łucka, M., Bereza, T., Białas, M. B., Pasternak, A., Crețoiu, D., Walocha, J. A., & Gil, K. (2019) · Cell Transplantation · doi:10.1177/0963689719833303 · Cited by 24 · see citing works
Fassbender, A., Simsa, P., Kyama, C. M., Waelkens, E., Mihalyi, A., Meuleman, C., Gevaert, O., Van de Plas, R., de Moor, B., & D'Hooghe, T. M. (2010) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-8-123 · Cited by 23 · see citing works
Hughes, C. L., Foster, W. G., & Agarwal, S. K. (2015) · BioMed Research International · doi:10.1155/2015/158490 · Cited by 23 · see citing works
Hey‐Cunningham, A. J., Markham, R., Fraser, I. S., & Berbic, M. (2013) · Reproductive Sciences · doi:10.1177/1933719113485299 · Cited by 22 · see citing works
Self-citationVasoactive intestinal peptide is upregulated in women with endometriosis and chronic pelvic pain
Bourlev, V., Moberg, C., Ilyasova, N. A., Davey, E., Kallak, T. K., & Olovsson, M. (2018) · American Journal of Reproductive Immunology · doi:10.1111/aji.12857 · Cited by 21 · see citing works
Fassbender, A., Dorien, O., Moor, B. D., Waelkens, E., Meuleman, C., Tomassetti, C., Peeraer, K., & D’Hooghe, T. M. (2014) · Springer eBooks · doi:10.1007/978-4-431-54421-0_20 · Cited by 22 · see citing works
Templeman, C. E. (2009) · Obstetrics and Gynecology Clinics of North America · doi:10.1016/j.ogc.2008.12.005 · Cited by 21 · see citing works
McAllister, S. L., Giourgas, B. K., Faircloth, E. K., Leishman, E., Bradshaw, H. B., & Gross, E. R. (2016) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.08.017 · Cited by 20 · see citing works
Ballester, M., Gonin, J., Rodenas, A., Bernaudin, J., Rouzier, R., Coutant, C., & Daraï, É. (2012) · Human Reproduction · doi:10.1093/humrep/des304 · Cited by 19 · see citing works
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
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
Margatho, D., Carvalho, N. M., Eloy, L., & Bahamondes, L. G. (2018) · The European Journal of Contraception & Reproductive Health Care · doi:10.1080/13625187.2018.1531117 · Cited by 17 · see citing works
Microanatomy and function of the eutopic endometrium in women with endometriosis
Al‐Jefout, M., Tokushige, N., Hey‐Cunningham, A. J., Manconi, F., Ng, C. H. M., Schulke, L., Berbic, M., Markham, R., & Is, F. (2008) · Expert Review of Obstetrics & Gynecology · doi:10.1586/17474108.4.1.61 · Cited by 15 · see citing works
Self-citationKaiser, A., Köpf, A., Gericke, C., Bartley, J., & Mechsner, S. (2009) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-008-0921-z · Cited by 13 · see citing works
Reduced sympathetic neurite outgrowth on uterine tissue sections from rats treated with estrogen
Richeri, A., Bianchimano, P., Crutcher, K. A., & Brauer, M. M. (2010) · Cell and Tissue Research · doi:10.1007/s00441-010-0956-x · Cited by 12 · see citing works
Коган, Е. А., Ovakimyan, A. S., Paramonova, N. B., Файзуллина, Н. М., Kozachenko, I. F., & Adamyan, L. V. (2016) · Russian Journal of Archive of Pathology · doi:10.17116/patol201678320-25 · Cited by 12 · see citing works
Endometriosis: The elusive epiphenomenon
Quinn, M. J. (2009) · Journal of Obstetrics and Gynaecology · doi:10.1080/01443610903082484 · Cited by 12 · see citing works
Preoperative assessment and diagnosis of endometriosis
Hirsch, M., & Davis, C. (2015) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/gco.0000000000000188 · Cited by 12 · see citing works
Advanced Insights into Human Uterine Innervation: Implications for Endometriosis and Pelvic Pain
Astruc, A., Roux, L., Robin, F., Sall, N. R., Dion, L., Lavoué, V., Legendre, G., Lévêque, J., Bessède, T., Bertrand, M. M., et al. (2024) · Journal of Clinical Medicine · doi:10.3390/jcm13051433 · Cited by 11 · see citing works
Loss of nerve fibers in the oviduct isthmus in women with hydrosalpinx
Zhu, L., Chen, J., Sun, Y., Huang, X., Xu, H., & Zhang, X. (2013) · Acta Histochemica · doi:10.1016/j.acthis.2013.01.008 · Cited by 11 · see citing works
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
Morphological identification of thoracolumbar spinal afferent nerve endings in mouse uterus
Dodds, K. N., Kyloh, M. A., Travis, L., Beckett, E. A. H., & Spencer, N. J. (2020) · The Journal of Comparative Neurology · doi:10.1002/cne.25070 · Cited by 10 · see citing works
Giray, B., Büyükbayrak, E. E., Keser, S. H., Karşıdağ, A. Y. K., & Türkgeldi, A. (2018) · Geburtshilfe und Frauenheilkunde · doi:10.1055/a-0591-1751 · Cited by 8 · see citing works
Chen, Y., Li, D., Zhang, Z., Takushige, N., Kong, B., & Wang, G. (2015) · PubMed Central · doi:10.22074/ijfs.2015.4211 · Cited by 8 · see citing works
Chronic pelvic pain in women: role of the nervous system
Gillett, W. R., & Jones, D. (2009) · Expert Review of Obstetrics & Gynecology · doi:10.1586/17474108.4.2.149 · Cited by 7 · see citing works
mRNA and miRNA Biomarkers for Endometriosis
Aghajanova, L., Burney, R. O., Tran, N. D., & Giudice, L. C. (2017) · Springer eBooks · doi:10.1007/978-3-319-59856-7_9 · Cited by 6 · see citing works
Dolci, C., Gautier, E. J. D., Lannez, L., Lebuffe, G., Wattier, J., & Rubod, C. (2025) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-025-08178-1 · Cited by 5 · see citing works
Endometrial nerve fibres in endometriosis
Tokushige, N., Al‐Jefout, M., Salih, H., & Fraser, I. S. (2007) · Bioline International (Bioline International) · Cited by 5 · see citing works
Self-citationDistribution 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
Manconi, F., Fazleabas, A. T., Markham, R., & Fraser, I. S. (2018) · Journal of Endometriosis and Pelvic Pain Disorders · doi:10.1177/2284026518810594 · Cited by 5 · see citing works
Self-citationGuan, Q., Velho, R. V., Jordan, A., Pommer, S., Radde, I., Sehouli, J., & Mechsner, S. (2023) · Cells · doi:10.3390/cells12101395 · Cited by 4 · see citing works
Daily Variation of Plasma Brain-derived Neurotrophic Factor in Women with Endometriosis
Bucci, F., Pluchino, N., Luisi, S. V., Cela, V., Artini, P. G., Giannini, A., Russo, M., Russo, N., Casarosa, E., Luisi, M., et al. (2011) · Journal of Endometriosis and Pelvic Pain Disorders · doi:10.5301/je.2011.8313 · Cited by 3 · see citing works
Cyclic Changes of Nerve Fibers in Human Endometrium
Tomita, T., & Mah, K. (2014) · Open Journal of Pathology · doi:10.4236/ojpathology.2014.42011 · Cited by 3 · see citing works
The diagnosis of endometriosis with the help of mass spectrometry (a review)
Borisova, A. V., Kozachenko, K. A. V., Starodubtseva, N. L., Бугрова, А. Е., Евгеньевич, Ф. В., & Adamjan, L. V. (2015) · Russian Journal of Human Reproduction · doi:10.17116/repro201521659-68 · Cited by 3 · see citing works
- Authors
- Tokushige, N., Markham, R., Russell, P., & Fraser, I. S.
- Affiliations
- The University of Sydney (AU)
- Corresponding author
- Tokushige, Natsuko
- Venue
- Fertility and Sterility
- Publisher
- Elsevier BV
- Published
- 2007-10
- Volume
- 88
- Issue
- 4
- Pages
- 795-803
- ISSN
- 0015-0282 (ISSN-L)
- OpenAlex
- W1994988244
- Cited by
- 151
- References
- 67
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 7 · 2023: 5 · 2022: 11 · 2021: 2 · 2020: 2 · 2019: 4 · 2018: 7 · 2017: 4 · 2016: 7 · 2015: 13 · 2014: 9 · 2013: 11 · 2012: 9
- FWCI
- 16.58
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Fertility and Sterility (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Health Sciences › Medicine › Obstetrics and Gynecology › Gynecological conditions and treatments
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Plant and fungal interactions
- Keywords
- endometriosis, endometrium, myometrium, nerve fiber density, adrenergic nerve fibers, cholinergic fibers, PGP 9.5, neurofilaments, substance P, calcitonin gene-related peptide, tyrosine hydroxylase, vesicular acetylcholine transporter, neuropeptides, endometriosis-associated pain, eutopic endometrium
- MeSH terms
- Adult, Endometriosis, Endometrium, Female, Humans, Hysterectomy, Immunohistochemistry, Myometrium, Nerve Fibers
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
