The Pains of Endometriosis
Abstract
Endometriosis is a disease defined by the presence of endometrial tissue outside of the uterus. Severe pelvic pain is often associated with endometriosis, and this pain can be diminished with therapies that suppress estrogen production. Many women with endometriosis also suffer from other chronic pain conditions. Recent studies suggest that mechanisms underlying these pains and sensitivity to estrogen involve the growth into the ectopic endometrial tissue of a nerve supply, which could have a varied and widespread influence on the activity of neurons throughout the central nervous system.
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Sensory fibers whose branches innervate ectopic growths immunostain with antibodies to calcitonin gene-related peptide, indicating that CGRP-positive fibers include C-fiber nociceptors.
“Sensory fibers whose branches innervate ectopic growths immunostain with antibodies to calcitonin gene-related peptide (CGRP) (Berkley et al., 2004(Berkley et al., , 2005)), indicating that the CGRP-positive fibers include C-fiber nociceptors (Snider and McMahon, 1998).”
From Chronic pelvic pain and endometriosis: translational evidence of the relationship and implications (2011) · cites this paper as Berkley et al., 2005
The characteristics of the newly formed nerve supply of ectopic growths and two-way communication between the growths and the central nervous system contribute to the variable association between growths and pain.
“characteristics of the ectopic growths' newly formed nerve supply and resultant two-way communication between the growths and CNS contribute to the variable association between the growths and pain”
From Chronic pelvic pain and endometriosis: translational evidence of the relationship and implications (2011) · cites this paper as Berkley et al., 2005
Sensory and sympathetic fibers directly innervate ectopic endometrial growths in a rat model and in lesions from women.
“Direct innervation of ectopic endometrial growths by sensory and sympathetic fibers was shown in endometriosis growths from a rat model (Berkley et al., 2004) and lesions from women (Berkley et al., 2005).”
From Chronic pelvic pain and endometriosis: translational evidence of the relationship and implications (2011) · cites this paper as Berkley et al., 2005
Ectopic growths from ENDO rats and women with established endometriosis develop their own C-fiber (sensory afferent) and sympathetic nerve supply.
“Our group discovered that ectopic growths harvested from ENDO rats and women with established endometriosis develop their own C-fiber (sensory afferent) and sympathetic (autonomic efferent) nerve supply.”
From Sprouted Innervation into Uterine Transplants Contributes to the Development of Hyperalgesia in a Rat Model of Endometriosis (2012) · cites this paper as [11]
The nerve supply to ectopic growths is derived from nerve fibers innervating nearby territories that sprout branches into the growths.
“The supply is derived from nerve fibers innervating nearby territories that sprout branches into the growths [10], [11].”
From Sprouted Innervation into Uterine Transplants Contributes to the Development of Hyperalgesia in a Rat Model of Endometriosis (2012) · cites this paper as [11]
In the rat ENDO model, the innervation of ectopic growths consists of branches of axons that sprout from pre-existing sensory neurons whose cell bodies are located in thoracic dorsal root ganglia (DRG) and from sympathetic neurons whose cell bodies are located in the coeliac ganglion (CG).
“This innervation in the rat model, diagrammed in Fig. 1b, consists of branches of axons that sprout from pre-existing sensory neurons whose cell bodies are located in thoracic dorsal root ganglia (DRG) and from sympathetic neurons whose cell bodies are located in the coeliac ganglion (CG).”
From Endocannabinoid involvement in endometriosis. (2010) · cites this paper as [5]
The ectopic growths in both the rat model and in women recruit their own sensory and sympathetic nerve supply.
“The ectopic growths in both the rat model and in women recruit their own sensory and sympathetic nerve supply [4,5].”
From Endocannabinoid involvement in endometriosis. (2010) · cites this paper as [5]
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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
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Fauconnier, A., Staraci, S., Huchon, C., Roman, H., Panel, P., & Descamps, P. (2013) · Human Reproduction · doi:10.1093/humrep/det310 · Cited by 94 · see citing works
Elevated peritoneal expression and estrogen regulation of nociceptive ion channels in endometriosis
Greaves, E., Grieve, K., Horne, A. W., & Saunders, P. T. K. (2014) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2014-2282 · Cited by 89 · see citing works
Antiproliferative Effects of Cannabinoid Agonists on Deep Infiltrating Endometriosis
Leconte, M., Nicco, C., Ngô, C., Arkwright, S., Chéreau, C., Guibourdenche, J., Weill, B. J., Chapron, C., Dousset, B. E., & Batteux, F. (2010) · American Journal Of Pathology · doi:10.2353/ajpath.2010.100375 · Cited by 85 · see citing works
Hyperinnervation 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
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
Examining subjective wellbeing and health-related quality of life in women with endometriosis
Rush, G., & Misajon, R. (2017) · Health Care For Women International · doi:10.1080/07399332.2017.1397671 · Cited by 83 · see citing works
Association of Central Sensitization Inventory Scores With Pain Outcomes After Endometriosis Surgery
Orr, N. L., Huang, A. J., Liu, Y. D., Noga, H. L., Bedaiwy, M. A., Williams, C., Allaire, C., & Yong, P. J. (2023) · JAMA Network Open · doi:10.1001/jamanetworkopen.2023.0780 · Cited by 80 · see citing works
“The exclusion criteria for participants included (1) postmenopausal status (spontaneous or surgical); (2) previous hysterectomy and/or bilateral salpingo-oophorectomy (before the baseline visit); (3) missing CSI or CPP scores; (4) follow-up completed less than 4 months after surgery; and (5) withdrawn consent.”
BackgroundMethodBerkley, 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-citationEvidence 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
“The presence of nerve fibers in direct contact to peritoneal, ovarian and deep infiltrating endometriosis has recently been confirmed [11,29,38], as well as the de novo innervation of peritoneal”
BackgroundZhang, 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-citationNeural involvement in endometriosis: Review of anatomic distribution and mechanisms
Siquara De Sousa, A. C., Capek, S., Amrami, K. K., & Spinner, R. J. (2015) · Clinical Anatomy · doi:10.1002/ca.22617 · Cited by 77 · see citing works
Indraccolo, U., & Barbieri, F. (2010) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2010.01.008 · Cited by 76 · see citing works
“It has been reported [8,10] that endometriotic nodules with rich innervation can be particularly algogenic due to chronic nociceptive hyperactivation at both peripheral and central levels [1], which explains the hyperaesthesia and allodynia experienced by patients even in the absence of pain symptoms.”
BackgroundMAP kinases and the inflammatory signaling cascade as targets for the treatment of endometriosis?
Santulli, P., Marcellin, L., Tosti, C., Chouzenoux, S., Cerles, O., Borghese, B., Batteux, F., & Chapron, C. (2015) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.2015.1090974 · Cited by 75 · see citing works
Estrogen modulation of ovariectomy‐induced hyperalgesia in adult mice
Sanoja, R., & Cerveró, F. (2007) · European Journal of Pain · doi:10.1016/j.ejpain.2007.09.003 · Cited by 73 · see citing works
Yu, J., Francisco, A. M. C., Patel, B. G., Cline, J. M., Zou, E., Berga, S. L., & Taylor, R. N. (2018) · American Journal Of Pathology · doi:10.1016/j.ajpath.2018.06.011 · Cited by 72 · see citing works
Nerve fibres in ovarian endometriotic lesions in women with ovarian endometriosis
Zhang, X., Yao, H., Huang, X., Lü, B., Xu, H., & Zhou, C. (2009) · Human Reproduction · doi:10.1093/humrep/dep427 · Cited by 72 · see citing works
Insights into assessing the genetics of endometriosis
Rahmioglu, N., Missmer, S. A., Montgomery, G. W., & Zondervan, K. T. (2012) · Current Obstetrics and Gynecology Reports · doi:10.1007/s13669-012-0016-5 · Cited by 71 · see citing works
Khan, K. N., Kitajima, M., Fujishita, A., Hiraki, K., Matsumoto, A., Nakashima, M., & Masuzaki, H. (2012) · Human Reproduction · doi:10.1093/humrep/des364 · Cited by 70 · see citing works
“Different mechanisms have been proposed to explain the relationship that exists between endometriosis and pelvic pain such as tissue inflammatory reaction, production of prostaglandins (PGs) with consequent uterine contraction and nerve entrapment within lesions (Anaf et al., 2000; Khan et al., 2004a; Berkley et al.,…”
BackgroundmiRNAs Regulation and Its Role as Biomarkers in Endometriosis
Marí‐Alexandre, J., Sánchez-Izquierdo, D., Gilabert–Estellés, J., Barceló‐Molina, M., Braza‐Boïls, A., & Sandoval, J. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17010093 · Cited by 71 · see citing works
Endometriosis of the urinary tract in women of reproductive age
Schneider, A. W., Touloupidis, S., Papatsoris, A., Triantafyllidis, A., Κόλλιας, Α., & Schweppe, K.-W. (2006) · International Journal of Urology · doi:10.1111/j.1442-2042.2006.01437.x · Cited by 70 · see citing works
Sperschneider, M. L., Hengartner, M. P., Schwartz, A. K., Geraedts, K., Rauchfuß, M., Woelfler, M. M., Haeberlin, F., von Orelli, S., Eberhard, M., Maurer, F., et al. (2019) · BMJ Open · doi:10.1136/bmjopen-2017-019570 · Cited by 70 · see citing works
Dyschezia and Posterior Deep Infiltrating Endometriosis: Analysis of 360 Cases
Seracchioli, R., Mabrouk, M., Guerrini, M., Manuzzi, L., Savelli, L., Frascà, C., & Venturoli, S. (2008) · Journal of Minimally Invasive Gynecology · doi:10.1016/j.jmig.2008.07.005 · Cited by 69 · see citing works
“According to the results of several studies, mechanisms responsible for severity of painful symptoms associated with endometriosis may include the interaction among ectopic endometriotic implant, nociceptors, and nerve fibers [1,12,17].”
Evans, S., Moalem‐Taylor, G., & Tracey, D. J. (2007) · Pain · doi:10.1016/j.pain.2007.07.006 · Cited by 68 · see citing works
Maulitz, L., Stickeler, E., Stickel, S., Habel, U., Tchaikovski, S. N., & Chechko, N. (2022) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2022.100988 · Cited by 67 · see citing works
“The nerve fibers within endometriotic lesions (Berkley et al., 2005) are permanently stimulated by inflammatory mediators and nerve-sensitizing proteins, which are released by noxious stimuli into the sensory afferent nerve at the lesion’s distal end with the nociceptive signal being transferred to the nerve root of t…”
Endometriosis: Update of Pathophysiology, (Epi) Genetic and Environmental Involvement
Monnin, N., Fattet, A.-J., & Koscinski, I. (2023) · Biomedicines · doi:10.3390/biomedicines11030978 · Cited by 67 · see citing works
“The concomitant development of nerve fibers explains the pain experienced by patients [3,43].”
BackgroundWomen with Endometriosis Are More Likely to Suffer from Migraines: A Population-Based Study
Yang, M.-H., Wang, P., Wang, S., Sun, W., Oyang, Y.-J., & Fuh, J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033941 · Cited by 67 · see citing works
Kajitani, T., Maruyama, T., Asada, H., Uchida, H., Oda, H., Nishikawa-Uchida, S., Miyazaki, K., Arase, T., Ono, M., & Yoshimura, Y. (2013) · Endocrine Journal · doi:10.1507/endocrj.ej13-0027 · Cited by 67 · see citing works
Phan, V. T., Stratton, P., Tandon, H. K., Sinaii, N., Aredo, J. V., Karp, B. I., Merideth, M. A., & Shah, J. P. (2020) · European Journal of Pain · doi:10.1002/ejp.1713 · Cited by 64 · 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
Self-citationRelationship between site and size of bladder endometriotic nodules and severity of dysuria
Villa, G., Mabrouk, M., Guerrini, M., Mignemi, G., Montanari, G., Fabbri, E., Venturoli, S., & Seracchioli, R. (2007) · Journal of Minimally Invasive Gynecology · doi:10.1016/j.jmig.2007.04.015 · Cited by 63 · see citing works
- Authors
- Berkley, K. J., Rapkin, A. J., & Papka, R. E.
- Affiliations
- Florida State University (US)
- ORCID
- Rapkin, Andrea J.
- Venue
- Science
- Published
- 2005-06-10
- Volume
- 308
- Issue
- 5728
- Pages
- 1587-1589
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W2068756641
- Cited by
- 455
- References
- 20
- Citations by year
- 2026: 9 · 2025: 13 · 2024: 17 · 2023: 20 · 2022: 21 · 2021: 21 · 2020: 31 · 2019: 21 · 2018: 22 · 2017: 16 · 2016: 21 · 2015: 26 · 2014: 20 · 2013: 23 · 2012: 28
- FWCI
- 24.18
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Diabetes and Digestive and Kidney Diseases (R21DK063937)
- National Institute of Neurological Disorders and Stroke (R01-NS-11892, R01 NS22526, R01NS022526, R01NS011892)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Health Sciences › Medicine › Physiology › Pain Mechanisms and Treatments
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Menstrual Health and Disorders
- Keywords
- endometriosis, pelvic pain, chronic pain, estrogen sensitivity, ectopic endometrium, innervation, central nervous system neurons, pain mechanisms
- MeSH terms
- Animals, Central Nervous System, Endometriosis, Female, Humans, Gonadotropin-Releasing Hormone, Neural Pathways, Neurons, Neurons, Afferent, Pain, Spinal Cord, Sympathetic Nervous System, Rats
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