Endometriosis-induced vaginal hyperalgesia in the rat: Role of the ectopic growths and their innervation
Open accessAbstract
Endometriosis is a painful disorder defined by extrauteral endometrial growths whose contribution to pain symptoms is poorly understood. Endometriosis is created in rats by autotransplanting on abdominal arteries pieces of either uterus (ENDO), which form cysts, or fat (shamENDO), which do not form cysts. ENDO, but not shamENDO induces vaginal hyperalgesia. We tested the hypothesis that the cysts are necessary to maintain vaginal hyperalgesia by assessing the effect of surgically removing them. Complete-cyst-removal eliminated ENDO-induced vaginal hyperalgesia up to 4 months post-operatively. Sham-cyst-removal in ENDO rats, in which cysts were not removed, or partial cyst-removal increased the ENDO-induced hyperalgesia. The decreases and increases both took 3-6 weeks to develop. Changes in ENDO-induced hyperalgesia did not occur in a control group of ENDO rats who had no surgery after ENDO. In a double-surgery control group, neither shamENDO surgery nor a subsequent sham surgery that mimicked "removal" of non-existent cysts influenced vaginal nociception. In a no-surgery control group, vaginal nociception remained stable for >6 months. The increases in ENDO-induced hyperalgesia produced by the sham-cyst-removal surgery were smaller in proestrus than in other estrous stages. During the other stages (but not during proestrus), sympathetic innervation of the cysts increased. These results suggest that maintenance of ENDO-induced vaginal hyperalgesia requires continued presence of at least some ectopic endometrial tissue, and that surgical treatment that fails to remove ectopic endometrial tissue can exacerbate the hyperalgesia, possibly due in part to an increase in the cysts' sympathetic innervation.
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Completely removing cysts abolishes endometriosis-induced vaginal hyperalgesia, but it returns when rats undergo reproductive senescence.
“Third, completely removing the cysts abolishes ENDO-induced vaginal hyperalgesia, but returns when rats undergo reproductive senescence (McAllister et al., 2009) at which time their estradiol levels, unlike women and mice, increase significantly (Lu et al., 1979;Berkley et al., 2007).”
From Chronic pelvic pain and endometriosis: translational evidence of the relationship and implications (2011) · cites this paper as McAllister et al., 2009
The Discussion (§4.1; page unavailable) says complete cyst removal eliminated vaginal hyperalgesia in the rats studied. It also reports a previous finding that removal during the transition into estropause did not prevent later increases in hyperalgesia. That does not establish the claimed sequence in which hyperalgesia was abolished and then returned in those rats. (LLM, conf=0.83)
Experimental — accuracy not yet measuredEndometriosis-induced vaginal hyperalgesia increases when cysts are incompletely removed.
“Fourth, ENDO-induced vaginal hyperalgesia increases when cysts are incompletely removed (McAllister et al., 2009).”
From Chronic pelvic pain and endometriosis: translational evidence of the relationship and implications (2011) · cites this paper as McAllister et al., 2009
The amount of cystic growth does not correlate with hyperalgesic severity in ENDO rats.
“the amount of cystic growth does not correlate with hyperalgesic severity [8], [9].”
From Sprouted Innervation into Uterine Transplants Contributes to the Development of Hyperalgesia in a Rat Model of Endometriosis (2012) · cites this paper as [9]
When a failure to remove all cysts during surgery produces an increase in hyperalgesia, that increase is accompanied by an increase in the density of sympathetic fibers in the cysts.
“Similarly, at that time, when a failure to remove all cysts during surgery produces an increase in hyperalgesia, that increase is accompanied by an increase in the density of sympathetic fibers in the cysts [9].”
From Sprouted Innervation into Uterine Transplants Contributes to the Development of Hyperalgesia in a Rat Model of Endometriosis (2012) · cites this paper as [9]
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Cites
Giudice, L. C., & Kao, L. C. (2004) · The Lancet · doi:10.1016/s0140-6736(04)17403-5 · Cited by 3,166 · see citing works
Knobil and Neill's Physiology of Reproduction
(2015) · Elsevier eBooks · doi:10.1016/c2011-1-07288-0 · Cited by 1,276 · see citing works
Strategies and Methods for Research on Sex Differences in Brain and Behavior
Becker, J. B., Arnold, A. P., Berkley, K. J., Blaustein, J. D., Eckel, L. A., Hampson, E., Herman, J. P., Marts, S. A., Sadée, W., Steiner, M. S., et al. (2004) · Endocrinology · doi:10.1210/en.2004-1142 · Cited by 799 · see citing works
Self-citationJi, R., & Woolf, C. J. (2001) · Neurobiology of Disease · doi:10.1006/nbdi.2000.0360 · Cited by 734 · see citing works
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
Studies on the surgical induction of endometriosis in the rat.
Vernon, M. W., & Wilson, E. A. (1985) · Fertility and Sterility · doi:10.1016/s0015-0282(16)48988-0 · Cited by 482 · see citing works
Berkley, K. J., Rapkin, A. J., & Papka, R. E. (2005) · Science · doi:10.1126/science.1111445 · Cited by 455 · see citing works
Self-citationImmune and glial cell factors as pain mediators and modulators
McMahon, S. B., Cafferty, W. B. J., & Marchand, F. (2005) · Experimental Neurology · doi:10.1016/j.expneurol.2004.11.001 · Cited by 441 · see citing works
Abbott, J. A. (2003) · Human Reproduction · doi:10.1093/humrep/deg275 · Cited by 403 · see citing works
Lu, K. H., HOPPER, B. R., Vargo, T. M., & Yen, S. S. C. (1979) · Biology of Reproduction · doi:10.1095/biolreprod21.1.193 · Cited by 402 · see citing works
Central Neuroplasticity and Pathological Pain
Melzack, R., Coderre, T. J., Katz, J. D., & Vaccarino, A. L. (2001) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2001.tb05822.x · Cited by 373 · see citing works
Neuroimmune activation and neuroinflammation in chronic pain and opioid tolerance/hyperalgesia
Deleo, J. A., Tanga, F. Y., & Tawfik, V. L. (2004) · The Neuroscientist · doi:10.1177/1073858403259950 · Cited by 371 · see citing works
Surgical Treatment of Endometriosis: A 7-Year Follow-up on the Requirement for Further Surgery
Shakiba, K., Bena, J. F., McGill, K. M., Minger, J., & Falcone, T. (2008) · Obstetrics & Gynecology · doi:10.1097/aog.0b013e3181758ec6 · Cited by 339 · see citing works
NGF as a mediator of inflammatory pain
McMahon, S. B. (1996) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1996.0039 · Cited by 332 · see citing works
Neuroendocrine Control of the Ovarian Cycle of the Rat
Freeman, M. R. (2006) · Elsevier eBooks · doi:10.1016/b978-012515400-0/50048-8 · Cited by 285 · see citing works
Neuron–glia crosstalk gets serious: role in pain hypersensitivity
Ren, K., & Dubner, R. A. (2008) · Current Opinion in Anaesthesiology · doi:10.1097/aco.0b013e32830edbdf · Cited by 271 · see citing works
Jänig, W., Levine, J. D., & Michaelis, M. (1996) · Progress in brain research · doi:10.1016/s0079-6123(08)61087-0 · Cited by 260 · see citing works
Pain, mast cells, and nerves in peritoneal, ovarian, and deep infiltrating endometriosis
Anaf, V., Chapron, C., El Nakadi, I., De Moor, V., Simonart, T., & Noël, J.-C. (2006) · Fertility and Sterility · doi:10.1016/j.fertnstert.2006.03.057 · Cited by 258 · see citing works
Weihe, E., Schäfer, M. K.-H., Erickson, J. D., & Eiden, L. E. (1994) · Journal of Molecular Neuroscience · doi:10.1007/bf02736730 · Cited by 230 · 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
Self-citationErnsberger, U. (2009) · Cell and Tissue Research · doi:10.1007/s00441-009-0784-z · Cited by 194 · see citing works
Characterization of rodent models of HIV-gp120 and anti-retroviral-associated neuropathic pain
Wallace, V. C. J., Blackbeard, J., Segerdahl, A. R., Hasnie, F., Pheby, T., McMahon, S. B., & Rice, A. S. C. (2007) · Brain · doi:10.1093/brain/awm195 · Cited by 176 · see citing works
Gibbs, G. F., Drummond, P. D., Finch, P. M., & Phillips, J. K. (2008) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.2007.04862.x · Cited by 116 · see citing works
Repeated sound stress enhances inflammatory pain in the rat
Khasar, S. G., Green, P. G., & Levine, J. D. (2005) · Pain · doi:10.1016/j.pain.2005.03.040 · Cited by 114 · see citing works
Estrogen Regulates Vaginal Sensory and Autonomic Nerve Density in the Rat1
Ting, A. Y., Blacklock, A. D., & Smith, P. G. (2004) · Biology of Reproduction · doi:10.1095/biolreprod.104.030023 · Cited by 112 · see citing works
Estrous changes in vaginal nociception in a rat model of endometriosis
Cason, A. M., Samuelsen, C. L., & Berkley, K. J. (2003) · Hormones and Behavior · doi:10.1016/s0018-506x(03)00121-1 · Cited by 94 · see citing works
Self-citationUsing Rats as a Research Model for the Study of Endometriosis
Sharpe-Timms, K. L. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb02792.x · Cited by 90 · see citing works
Estrous variations in behavioral responses to vaginal and uterine distention in the rat
Bradshaw, H. B., Temple, J. L., Wood, E., & Berkley, K. J. (1999) · Pain · doi:10.1016/s0304-3959(99)00049-4 · Cited by 90 · see citing works
Self-citationBerkley, K. J., McAllister, S. L., Accius, B. E., & Winnard, K. P. (2007) · Pain · doi:10.1016/j.pain.2007.09.022 · Cited by 80 · see citing works
Self-citationZhang, G., Dmitrieva, N., Liu, Y., McGinty, K. A., & Berkley, K. J. (2008) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00649.2007 · Cited by 78 · see citing works
Self-citation(2008) · Obstetrics and Gynecology · doi:10.1097/aog.0b013e318188d29c · Cited by 78 · see citing works
Nitric oxide nerves in the uterus are parasympathetic, sensory, and contain neuropeptides
Papka, R. E., McNeill, D. L., Thompson, D., & Schmidt, H. H. H. W. (1995) · Cell and Tissue Research · doi:10.1007/bf00318490 · Cited by 67 · see citing works
Behavioral responses to uterine or vaginal distension in the rat
Berkley, K. J., Wood, E., Scofield, S. L., & Little, M. (1995) · Pain · doi:10.1016/0304-3959(94)00150-d · Cited by 60 · see citing works
Self-citationEstrogen replacement reverses ovariectomy-induced vaginal hyperalgesia in the rat
Bradshaw, H. B., & Berkley, K. J. (2002) · Maturitas · doi:10.1016/s0378-5122(01)00261-4 · Cited by 54 · see citing works
Self-citationOvariohysterectomy in the rat: a model of surgical pain for evaluation of pre-emptive analgesia?
González, M. I., Field, M. J., Bramwell, S., McCleary, S., & Singh, L. (2000) · Pain · doi:10.1016/s0304-3959(00)00309-2 · Cited by 50 · see citing works
Nagabukuro, H., & Berkley, K. J. (2007) · Pain · doi:10.1016/j.pain.2007.04.039 · Cited by 47 · see citing works
Self-citationAutonomic Fiber Sprouting in the Skin in Chronic Inflammation
Almarestani, L., Longo, G., & Ribeiro‐da‐Silva, A. (2008) · Molecular Pain · doi:10.1186/1744-8069-4-56 · Cited by 43 · see citing works
Estrogen regulation of neurotrophin expression in sympathetic neurons and vascular targets
Kaur, G., Janik, J., Isaacson, L. G., & Callahan, P. (2007) · Brain Research · doi:10.1016/j.brainres.2006.12.084 · Cited by 39 · see citing works
Morrison, T. C., Dmitrieva, N., Winnard, K. P., & Berkley, K. J. (2006) · Fertility and Sterility · doi:10.1016/j.fertnstert.2006.03.026 · Cited by 35 · see citing works
Self-citationMorán, C., Franco, A., Morán, J. L., Handal‐Silva, A., Morales, L., & Domı́nguez, R. (2005) · Endocrine · doi:10.1385/endo:26:2:147 · Cited by 34 · see citing works
Treatment of endometriosis-related pain options and outcomes
Somigliana, E. (2009) · Frontiers in Bioscience-Elite · doi:10.2741/e41 · Cited by 29 · see citing works
Anglin, J. C., & Brooks, V. L. (2003) · Autonomic Neuroscience · doi:10.1016/s1566-0702(03)00020-1 · Cited by 29 · see citing works
Jesch, N. K., Kuebler, J. F., Nguyen, H., Nave, H., Bottländer, M., Teichmann, B., Braun, A. C., Vieten, G., & Ure, B. M. (2006) · Journal of Pediatric Surgery · doi:10.1016/j.jpedsurg.2006.02.002 · Cited by 22 · see citing works
(2009) · Oxford University Press eBooks · doi:10.1093/med/9780199235193.001.0001 · Cited by 14 · see citing works
Lee, T., Lin, M., & Chang, N. (2007) · Endocrinology · doi:10.1210/en.2007-0859 · Cited by 11 · see citing works
Mechanisms: lessons from translational studies of endometriosis
Berkley, K. J., & Stratton, P. (2009) · Visceral Pain · doi:10.1093/med/9780199235193.003.0005 · Cited by 5 · see citing works
Self-citationRita Levi-Montalcini: A brief biographic view of past and present studies on nerve growth factor
Aloe, L. (1999) · Microscopy Research and Technique · doi:10.1002/(sici)1097-0029(19990515/01)45:4/5 · Cited by 2 · see citing works
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- [15]Dmitrieva N Nikonov A Berkley KJ Endometriosis (ENDO) in the rat: sensitization of afferent fibers that innervate the ectopic growths Program No. xxx.x (in press), 2009 Neuroscience Meeting Planner Chicago, IL Society for Neuroscience 2009 Online
Cited by
Sorted by citations
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
Self-citationMaddern, 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
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
Phenotypic features of central sensitization
Williams, D. A. (2018) · Journal of Applied Biobehavioral Research · doi:10.1111/jabr.12135 · Cited by 180 · see citing works
Dual suppression of estrogenic and inflammatory activities for targeting of endometriosis
Zhao, Y., Gong, P., Chen, Y., Nwachukwu, J. C., Srinivasan, S., Ko, C., Bagchi, M. K., Taylor, R. N., Korach, K. S., Nettles, K. W., et al. (2015) · Science Translational Medicine · doi:10.1126/scitranslmed.3010626 · Cited by 170 · see citing works
He, W., Liu, X., Zhang, Y., & Guo, S. (2010) · Reproductive Sciences · doi:10.1177/1933719110381927 · Cited by 96 · see citing works
Greaves, E., Horne, A. W., Jerina, H., Mikolajczak, M., Hilferty, L., Mitchell, R., Fleetwood‐Walker, S., & Saunders, P. T. K. (2017) · Scientific Reports · doi:10.1038/srep44169 · Cited by 85 · see citing works
Yan, D., Liu, X., & Guo, S.-W. (2019) · Scientific Reports · doi:10.1038/s41598-019-39170-w · Cited by 82 · see citing works
Zheng, P., Wen, Z., Jinhua, L., & Jinghe, L. (2019) · Journal of Pain Research · doi:10.2147/jpr.s197667 · Cited by 90 · see citing works
Cuffaro, F., Russo, E., & Amedei, A. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25126473 · Cited by 82 · see citing works
Liu, M.-H., Liu, X., Zhang, Y., & Guo, S. (2012) · Reproductive Sciences · doi:10.1177/1933719111424453 · Cited by 68 · see citing works
Endocannabinoid involvement in endometriosis.
Dmitrieva, N., Nagabukuro, H., Resuehr, D., Zhang, G., McAllister, S. L., McGinty, K. A., Mackie, K., & Berkley, K. J. (2010) · Pain · doi:10.1016/j.pain.2010.08.037 · Cited by 64 · see citing works
“Findings from the rat model and clinical studies strongly support the conclusion that this innervation contributes to endometriosis-associated pain [21,35,48].”
BackgroundMethodResultSelf-citationMcAllister, S. L., Dmitrieva, N., & Berkley, K. J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031758 · Cited by 60 · see citing works
Self-citationEndometriosis-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
Pierce, A. N., Ryals, J. M., Wang, R., & Christianson, J. A. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.01.022 · Cited by 56 · see citing works
Pullen, 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
Iuvone, T., Affaitati, G., Filippis, D. D., Lopopolo, M., Grassia, G., Lapenna, D., Negro, L., Costantini, R., Vaia, M., Cipollone, F., et al. (2015) · Pain · doi:10.1097/j.pain.0000000000000220 · Cited by 42 · see citing works
Prediction of postoperative pain after gynecologic laparoscopy for nonacute pelvic pain
Jarrell, J. F., Ross, S., Robert, M., Wood, S. L., Tang, S., Stephanson, K., & Giamberardino, M. A. (2014) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2014.04.010 · Cited by 40 · see citing works
Ectopic uterine tissue as a chronic pain generator
Alvarez, P., Chen, X., Hendrich, J., Irwin, J. C., Green, P. G., Giudice, L. C., & Levine, J. D. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.08.033 · Cited by 39 · see citing works
Ge, P., Ren, J., Harrington, A. M., Grundy, L., Castro, J., Brierley, S. M., & Hannig, G. (2019) · Pain · doi:10.1097/j.pain.0000000000001657 · Cited by 39 · 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
Coxon, L., Wiech, K., & Vincent, K. (2021) · Frontiers in Pain Research · doi:10.3389/fpain.2021.743812 · Cited by 32 · see citing works
Estrogen up-regulation of semaphorin 3F correlates with sympathetic denervation of the rat uterus
Richeri, A., Chalar, C., Martínez, G. F., Greif, G., Bianchimano, P., & Brauer, M. M. (2011) · Autonomic Neuroscience · doi:10.1016/j.autneu.2011.06.002 · Cited by 26 · see citing works
Neuropelveology: An Emerging Discipline for the Management of Chronic Pelvic Pain
Possover, M., Andersson, K., & Forman, A. (2017) · International Neurourology Journal · doi:10.5213/inj.1735036.518 · Cited by 24 · see citing works
Dodds, K. N., Beckett, E. A. H., Evans, S., & Hutchinson, M. R. (2018) · Reproductive Sciences · doi:10.1177/1933719118773405 · Cited by 24 · see citing works
Castro, J., Maddern, J., Grundy, L., Manavis, J., Harrington, A. M., Schober, G., & Brierley, S. M. (2021) · The FASEB Journal · doi:10.1096/fj.202002441r · Cited by 24 · see citing works
Zheng, P., Jia, S., Guo, D., Chen, S., Zhang, W., Cheng, A., Xie, W., Sun, G., Leng, J., & Lang, J. (2020) · Journal of Pain Research · doi:10.2147/jpr.s232313 · Cited by 22 · see citing works
Oskotsky, T., Bhoja, A., Bunis, D. G., Le, B. L., Tang, A., Kosti, I., Li, C., Houshdaran, S., Sen, S., Vallvé-Juanico, J., et al. (2024) · iScience · doi:10.1016/j.isci.2024.109388 · Cited by 21 · see citing works
Self-citationTorres-Reverón, A., Palermo, K., Hernández-López, A., Hernández, S., Cruz, M. L., Thompson, K. J., Flores, I., & Appleyard, C. B. (2016) · Reproductive Sciences · doi:10.1177/1933719116630410 · 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
Self-citationFilho, P. W. L. L., Filho, A. J. M. C., Vieira, C. F. X., Oliveira, T. D. Q., Soares, M. V. R., Jucá, P. M., Quevedo, J., Barichello, T., Macêdo, D. S., & Medeiros, F. D. C. (2019) · Metabolic Brain Disease · doi:10.1007/s11011-019-00397-1 · Cited by 18 · see citing works
Chen, S., Xie, W., Strong, J. A., Jiang, J., & Zhang, J. ‐. (2015) · European Journal of Pain · doi:10.1002/ejp.827 · Cited by 18 · see citing works
Alali, Z., Graham, A. R., Swan, K., Flyckt, R. L., Falcone, T., Cui, W., Yang, X., Christianson, J. A., & Nothnick, W. B. (2019) · Molecular Human Reproduction · doi:10.1093/molehr/gaz065 · Cited by 17 · see citing works
Zhao, Y., Chen, Y., Kuang, Y., Bagchi, M. K., Taylor, R. N., Katzenellenbogen, J. A., & Katzenellenbogen, B. S. (2015) · Endocrinology · doi:10.1210/en.2015-1324 · Cited by 17 · see citing works
McAllister, S. L., Sinharoy, P., Vasu, M., & Gross, E. R. (2020) · Pain · doi:10.1097/j.pain.0000000000001949 · Cited by 16 · see citing works
Self-citationGreaves, 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
Castro, J., Maddern, J., Erickson, A., Caldwell, A., Grundy, L., Harrington, A. M., & Brierley, S. M. (2020) · Pain · doi:10.1097/j.pain.0000000000002036 · Cited by 14 · see citing works
Maddern, J., Grundy, L., Harrington, A. M., Schober, G., Castro, J., & Brierley, S. M. (2021) · Pain · doi:10.1097/j.pain.0000000000002552 · Cited by 13 · see citing works
Han, H., Liang, X., Wang, J., Zhao, Q., Yang, M., Rong, W., & Zhang, G. (2017) · Brain Research · doi:10.1016/j.brainres.2017.03.016 · Cited by 11 · 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
Impact of surgical excision of lesions on pain in a rat model of endometriosis
Álvarez, P., Giudice, L. C., & Levine, J. D. (2014) · European Journal of Pain · doi:10.1002/ejp.527 · Cited by 10 · see citing works
Burns, K. A., Peterse, D., Appleyard, C. B., Chandler, R. L., Guo, S., Pearson, A. M., Persoons, E., Anglesio, M. S., Rogers, M. S., Sharpe-Timms, K. L., et al. (2025) · Molecular Human Reproduction · doi:10.1093/molehr/gaaf021 · Cited by 9 · see citing works
Self-citationDodds, K. N., Fattori, V., Andrews, N. A., Appleyard, C. B., Christianson, J. A., Gomez, R., McAllister, S. L., Missmer, S. A., Nagel, J., Nuñez‐Badinez, P., et al. (2025) · Molecular Human Reproduction · doi:10.1093/molehr/gaaf023 · Cited by 9 · see citing works
Self-citationThe 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
The Clinical Presentation of Endometriosis and Its Association to Current Surgical Staging
Ashkenazi, M. S., Huseby, O. L., Kroken, G., Trocha, M., Henriksson, A., Jasiak-Jóźwik, H., Cuartas, K., Loschiavo, A., Kuhn, I., Støve, D., et al. (2023) · Journal of Clinical Medicine · doi:10.3390/jcm12072688 · Cited by 9 · see citing works
Stratton, P. (2014) · Human Reproduction · doi:10.1093/humrep/deu131 · Cited by 7 · see citing works
The Unmet Needs for Studying Chronic Pelvic/Visceral Pain Using Animal Models
Neto, A. C., Santos-Pereira, M., Abreu‐Mendes, P., Neves, D., Almeida, H., Cruz, F., & Charrua, A. (2023) · Biomedicines · doi:10.3390/biomedicines11030696 · Cited by 6 · see citing works
Not always lost in translation
Ness, T. J. (2013) · Pain · doi:10.1016/j.pain.2013.03.022 · Cited by 4 · see citing works
Hu, S., Guo, W., & Shen, Y. (2022) · International Immunopharmacology · doi:10.1016/j.intimp.2022.109452 · Cited by 3 · see citing works
The display of paced mating behavior in a rat model of endometriosis
Clark, A. S., Robinson, S., Boisvert, E., & Quill, K. A. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.07.022 · Cited by 2 · see citing works
Nuñez‐Badinez, P., Shah, R., Demetriou, L., Leo, B. D., Meijlink, J. M., Birch, J. V., Schmidt, N., Nagel, J., & Vincent, K. (2024) · Reproduction and Fertility · doi:10.1530/raf-23-0083 · Cited by 1 · see citing works
Oskotsky, T., Tang, X., Arthurs, E., Govil, A., Abbasi, F., Bhoja, A., Bunis, D. G., Lau, A., Einhaus, J. F., Diop, M., et al. (2026) · iScience · doi:10.1016/j.isci.2026.117153 · Cited by 1 · see citing works
Self-citationPelvic organ cross-talk: A new paradigm for endometriosis-related pelvic pain?
Monten, L., Forman, A., & Andersson, K. (2018) · Journal of Endometriosis and Pelvic Pain Disorders · doi:10.1177/2284026518810573 · Cited by 1 · see citing works
Neuroendocrine Aspects of Endometriosis‐Associated Pain
Stratton, P., & Berkley, K. J. (2011) · Wiley eBooks · doi:10.1002/9781444398519.ch22
Self-citationHyperalgesiemechanismen bei Patientinnen mit Endometriose
Möller, K. (2015) · Universitätsbibliothek der FU Berlin Hochschulschriftenstelle u. Dokumentenserver · doi:10.17169/refubium-7881
Silveira, P. P., Texidor-Frugoni, C., Martínez, G. F., & Brauer, M. M. (2016) · Autonomic Neuroscience · doi:10.1016/j.autneu.2016.09.016
Pre-clinical Models of Endometriosis: A Focus on Chronic Pain
Maddern, J., Brierley, S. M., & Castro, J. (2023) · Springer eBooks · doi:10.1007/978-3-031-25702-5_16
Advances in endometriosis research: animal models for the study of reproductive disorders
Zhou, M., Zhou, X., & Wang, X. (2025) · Biology of Reproduction · doi:10.1093/biolre/ioaf089
Minchella, P. M., Vashisht, A., Peterson, R., Graham, A. R., Gunewardena, S., Cui, W., Findley, A., Christianson, J. A., Chennathukuzhi, V. M., & Nothnick, W. B. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.05.30.728827
- Authors
- McAllister, S. L., McGinty, K. A., Resuehr, D., & Berkley, K. J.
- Affiliations
- Florida State University (US)
- Venue
- Pain
- Published
- 2009-12
- Volume
- 147
- Issue
- 1
- Pages
- 255-264
- ISSN
- 0304-3959 (ISSN-L)
- PMC
- PMC2787658
- OpenAlex
- W2033814351
- Cited by
- 59
- References
- 47
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 4 · 2023: 5 · 2022: 1 · 2021: 3 · 2020: 5 · 2019: 5 · 2018: 3 · 2017: 3 · 2016: 3 · 2015: 5 · 2014: 5 · 2013: 1 · 2012: 4
- FWCI
- 4.32
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Pain (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- NIH (RO1-NS11892)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Health Sciences › Medicine › Physiology › Pain Mechanisms and Treatments
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Plant and fungal interactions
- Keywords
- endometriosis, ectopic endometrium, endometriotic cysts, cyst excision, sympathetic innervation, estrous cycle, proestrus, endometriosis surgery, autologous transplantation
- MeSH terms
- Analysis of Variance, Animals, Disease Models, Animal, Endometriosis, Escape Reaction, Female, Hyperalgesia, Pain Measurement, Physical Stimulation, Time Factors, Transplantation, Autologous, Vagina, Pain Threshold, Pelvic Pain, Area Under Curve, Estrous Cycle, Rats
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.
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