Hyperalgesia, nerve infiltration and nerve growth factor expression in deep adenomyotic nodules, peritoneal and ovarian endometriosis
Abstract
BACKGROUND: The aim of this study was to investigate a possible role for nerve growth factor (NGF) in the mechanism of pain and hyperalgesia induced by deep adenomyotic nodules and other forms of endometriosis and to clarify the relationship between endometriotic lesions and the surrounding nerves. METHODS: Endometriotic lesions (deep adenomyotic nodules, peritoneal endometriosis, ovarian endometriosis) and eutopic endometrium were obtained from 51 patients presenting with pain. Patients were allocated to two groups (group 1: patients with a deep adenomyotic nodule (n = 23); group 2: patients with peritoneal and/or ovarian endometriosis but without deep adenomyotic nodule (n = 28). Immunohistochemistry with antibodies against NGF, NGF specific tyrosine-kinase receptor (Trk-A) and S-100 protein was performed. Results were expressed as mean H-scores +/- SD, and correlated with the presence of hyperalgesia. RESULTS: The percentage of patients presenting hyperalgesia at physical examination was significantly higher in group 1 (96%) than in group 2 (11%) (P < 0.001). NGF expression was significantly stronger in deep adenomyotic nodules (DAN) than in ovarian (OE) and peritoneal endometriosis (PE), both in the proliferative phase in the glands [DAN: 226 +/- 18; OE: 140 +/- 9 (P < 0.001); PE: 110 +/- 7 (P < 0.001)] and in the stroma [(DAN: 204 +/- 21; OE: 125 +/- 15 (P < 0.001); PE: 100 +/- 9 (P < 0.01)]. NGF expression in DAN is also significantly stronger than in OE and PE in the secretory phase in the glands [DAN:181 +/- 32; OE: 85 +/- 3.3 (P < 0.001); PE: 65 +/- 9 (P < 0.001)] and in the stroma [DAN: 173 +/- 28; OE: 85 +/- 3.7 (P < 0.001); PE: 35 +/- 13 (P < 0.001)]. Perineurial and intraneurial invasion by endometriotic lesions were found only in deep adenomyotic nodules and not in the other forms of endometriosis. The specific receptor for NGF (Trk-A) is expressed in all the nerves that were included in the biopsies. CONCLUSIONS: These results suggest a role of NGF in endometriotic pain and hyperalgesia in deep adenomyotic nodules. The strong expression of the NGF-TrkA pathway in deep adenomyotic nodules could explain why this type of lesion infiltrates in richly innervated anatomical sites.
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Nerve growth factor in lesions may contribute to pain, particularly in deep adenomyotic nodules, where it correlates with hyperalgesia defined as intense pain when pressure is applied to the posterior fornix.
“The presence of nerve growth factor (NGF) in lesions may be involved, especially in deep adenomyotic nodules where it correlates with hyperalgesia, defined as intense pain reported when pressure is exerted in the posterior fornix”
From Chronic pelvic pain and endometriosis: translational evidence of the relationship and implications (2011) · cites this paper as Anaf et al., 2002
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 [32]
Adenomyosis externa lesions occasionally invade nerves and have some neurotropic effect.
“These adenomyosis externa lesions occasionally invade nerves (14) and have some neurotropic effect (15,16).”
From Pathogenesis of deep endometriosis (2017) · cites this paper as [14]
The specific receptor Trk-A for NGF is expressed in nerves lying within deep lesions or in the vicinity of deep endometriotic lesions.
“Nerve growth factor (NGF), which plays a key role in the occurrence of pain, hyperalgesia, and neuropathic pain, is strongly expressed in deep infiltrating endometriosis, and its specific receptor (Trk-A) is expressed in nerves lying within deep lesions or in the vicinity of deep endometriotic lesions (9).”
From Pain, mast cells, and nerves in peritoneal, ovarian, and deep infiltrating endometriosis (2006) · cites this paper as [9]
Nerve growth factor (NGF) plays a key role in the occurrence of pain, hyperalgesia, and neuropathic pain.
“Nerve growth factor (NGF), which plays a key role in the occurrence of pain, hyperalgesia, and neuropathic pain, is strongly expressed in deep infiltrating endometriosis, and its specific receptor (Trk-A) is expressed in nerves lying within deep lesions or in the vicinity of deep endometriotic lesions (9).”
From Pain, mast cells, and nerves in peritoneal, ovarian, and deep infiltrating endometriosis (2006) · cites this paper as [9]
NGF is strongly expressed in deep infiltrating endometriosis.
“Nerve growth factor (NGF), which plays a key role in the occurrence of pain, hyperalgesia, and neuropathic pain, is strongly expressed in deep infiltrating endometriosis, and its specific receptor (Trk-A) is expressed in nerves lying within deep lesions or in the vicinity of deep endometriotic lesions (9).”
From Pain, mast cells, and nerves in peritoneal, ovarian, and deep infiltrating endometriosis (2006) · cites this paper as [9]
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- Authors
- Anaf, V., Simon, P., El Nakadi, I., Fayt, I., Simonart, T., Buxant, F., & Noel, J.-C.
- Affiliations
- Université Libre de Bruxelles (BE)
- Erasmus Hospital (BE)
- Venue
- Human Reproduction
- Publisher
- Oxford University Press (OUP)
- Published
- 2002-07-01
- Volume
- 17
- Issue
- 7
- Pages
- 1895-1900
- ISSN
- 0268-1161 (ISSN-L)
- 1460-2350
- OpenAlex
- W2110802986
- Semantic Scholar
- db2adb14c4bace7cd06b411d8a12f49a05c0981c
- Cited by
- 317
- References
- 29
- Citations by year
- 2026: 6 · 2025: 8 · 2024: 9 · 2023: 13 · 2022: 12 · 2021: 16 · 2020: 16 · 2019: 17 · 2018: 13 · 2017: 19 · 2016: 18 · 2015: 23 · 2014: 24 · 2013: 17 · 2012: 19
- FWCI
- 3.72
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Human Reproduction (publishedVersion)
- PubMed (publishedVersion)
- Dépôt institutionnel de l'Université libre de Bruxelles (Université Libre de Bruxelles) (submittedVersion)
- 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, hyperalgesia, nerve growth factor, S-100 protein, peritoneal endometriosis, endometrioma, nerve infiltration, endometrial stroma, menstrual cycle phases, eutopic endometrium, immunohistochemistry, tyrosine kinase inhibitors
- MeSH terms
- Adult, Endometriosis, Female, Humans, Hyperalgesia, Immunohistochemistry, Nervous System, Ovarian Diseases, Peritoneal Diseases, Nerve Growth Factor
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