Cited by 122Endometriosis Research and TreatmentGynecological conditions and treatmentsDiagnosis and treatment of tuberculosis

The DOI matches its Crossref record; 152 of the 153 references it cites were found in a registry or an index.

The Role of the Lymphatic System in Endometriosis: A Comprehensive Review of the Literature1

Jerman, Laila F., Hey-Cunningham, Alison J.·2015·Biology of Reproduction

DOI 10.1095/biolreprod.114.124313

Open this paper in CoChat — free account

Abstract

Endometriosis is a benign gynecological disorder characterized by the presence of tissue resembling the endometrium in locations outside the uterus. The pathogenesis of endometriosis is still unknown; however, it is believed that the lymphatic system plays major roles in the development and progression of the disease. The lymphatic dissemination theory has been proposed to explain the presence of endometrial and/or endometriotic tissue in lymphatic vessels, lymph nodes, and rare sites, as well as high reoccurrence rates following treatment. Despite the importance of the lymphatic system in many aspects of endometriosis, there has been no previous thorough scientific update on its role in the disease. A review of scientific literature on the lymphatic system, lymphangiogenesis, and immunological changes associated with endometriosis was conducted. Lymphangiogenic potential is disturbed and lymphatic vessel density increased in the eutopic endometrium of women with endometriosis, likely promoting the entry of endometrial tissues into the lymphatic circulation. Endometriotic lesions and endometrial-like cells are present in uterine-draining nodes and various other pelvic lymph nodes. Immune responses are impaired in uterine-draining nodes, likely favoring the survival of endometrial cells and lesion establishment. In addition, lymphangiogenesis in endometriotic lesions may contribute to lesion growth and persistence, and promote the spread of endometrial cells to draining lymph nodes. The evidence reviewed in this paper supports the theory of lymphatic dissemination of endometriosis and highlights the roles of the lymphatic system in the pathogenesis and persistence of endometriosis. Understanding these roles is crucial for establishment of novel therapeutic approaches.

Integrity signals

Registry

Crossref · 10.1095/biolreprod.114.124313

Cites

152 of 152 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

Detection of Circulating Tumor DNA in Early- and Late-Stage Human Malignancies
Bettegowda, C., Sausen, M., Leary, R. J., Kinde, I., Wang, Y., Agrawal, N., Bartlett, B. R., Wang, H., Luber, B., Alani, R. M., et al. (2014) · Science Translational Medicine · doi:10.1126/scitranslmed.3007094 · Cited by 5,067
Endometriosis
Giudice, L. C., & Kao, L. C. (2004) · The Lancet · doi:10.1016/s0140-6736(04)17403-5 · Cited by 3,166
Peritoneal endometriosis due to the menstrual dissemination of endometrial tissue into the peritoneal cavity
Sampson, J. A. (1927) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(15)30003-x · Cited by 2,334
Peritoneal endometriosis, ovarian endometriosis, and adenomyotic nodules of the rectovaginal septum are three different entities
Nisolle, M., & Donnez, J. (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)00191-x · Cited by 1,279
Metastatic or Embolic Endometriosis, due to the Menstrual Dissemination of Endometrial Tissue into the Venous Circulation.
(1927) · PubMed Central · Cited by 1,008
Untitled work
(1984) · PubMed · Cited by 997
Lymphangiogenesis and cancer metastasis
Stacker, S. A., Achen, M. G., Jussila, L., Baldwin, M. E., & Alitalo, K. K. (2002) · Nature reviews. Cancer · doi:10.1038/nrc863 · Cited by 798
The physiology of the lymphatic system
Swartz, M. A. (2001) · Advanced Drug Delivery Reviews · doi:10.1016/s0169-409x(01)00150-8 · Cited by 738
Recurrence of endometriosis and its control
Guo, S.-W. (2009) · Human Reproduction Update · doi:10.1093/humupd/dmp007 · Cited by 719
Lymphedema
Warren, A. G., Brorson, H., Borud, L. J., & Slavin, S. A. (2007) · Annals of Plastic Surgery · doi:10.1097/01.sap.0000257149.42922.7e · Cited by 683

Show all 153 references

Research works printed but not linked: 5

1898, Adenofibromyoma cysticum sarcomatoides carcinomatosum, Monatschr Geburtshilfe Gynakol, 7, 295
2009, and function of the eutopic endometrium in women with endometriosis, Expert Rev, 4, 61
2004, terBrugge KG, Gentili F, Halliday W. Cerebellar endometriosis, AJR Am J Roentgenol, 182, 1543
2006, Endometriosis-related endometrial dysfunctions, World Endometr Soc, 8, 7
2007, Expressions of insulin-like growth factor I and its receptor in endometriosis, J Jilin Univ, 33, 567

Sorted by citations

Endometriosis
Zondervan, K. T., Becker, C. M., & Missmer, S. A. (2020) · New England Journal of Medicine · doi:10.1056/nejmra1810764 · Cited by 2,249
Rethinking mechanisms, diagnosis and management of endometriosis
Chapron, C., Marcellin, L., Borghese, B., & Santulli, P. (2019) · Nature Reviews Endocrinology · doi:10.1038/s41574-019-0245-z · Cited by 1,084
The endometrial immune environment of women with endometriosis
Vallvé-Juanico, J., Houshdaran, S., & Giudice, L. C. (2019) · Human Reproduction Update · doi:10.1093/humupd/dmz018 · Cited by 533
Pathogenesis of endometriosis: The genetic/epigenetic theory
Koninckx, P. R., Ussia, A., Adamyan, L., Wattiez, A., Gomel, V., & Martin, D. C. (2019) · Fertility and Sterility · doi:10.1016/j.fertnstert.2018.10.013 · Cited by 427
“These lesions are generally unique, larger than 1 cm in diameter, with frequent invasion into the muscle of the bowel wall, and with occasional nerve invasion (22), a neurotropic effect (23, 24), and some 20% lymph node involvement (25, 26).”
Background
The Main Theories on the Pathogenesis of Endometriosis
Lamceva, J., Uljanovs, R., & Strumfa, I. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24054254 · Cited by 324
“The benefit of a benign metastasis theory is that this pathogenetic mechanism can explain the occurrence of endometriosis in lymphatic nodes and distant locations such as lungs, because lymphatic capillaries are found in almost all organs [14].”
Background
Extrapelvic Endometriosis: A Systematic Review
Andres, M. P., Arcoverde, F. V. L., Souza, C. C. C., Fernandes, L. F. C., Abrão, M. S., & Kho, R. M. (2020) · Journal of Minimally Invasive Gynecology · doi:10.1016/j.jmig.2019.10.004 · Cited by 276
Pathogenesis of deep endometriosis
Gordts, S., Koninckx, P., & Brosens, I. (2017) · Fertility and Sterility · doi:10.1016/j.fertnstert.2017.08.036 · Cited by 241
Molecular and Cellular Pathogenesis of Endometriosis
Klemmt, P. A. B., & Starzinski‐Powitz, A. (2017) · Current Women s Health Reviews · doi:10.2174/1573404813666170306163448 · Cited by 182
“Further dispersion of endometrial cells via the lymphatic systems [22, 23] and reviewed in [24] might be the origin of lesions at more distant locations such as thoracic or cerebellar endometriosis [10, 25, 26].”
Background
Pharmaceuticals targeting signaling pathways of endometriosis as potential new medical treatment: A review
Hung, S. W., Zhang, R., Tan, Z., Chung, J. P. W., Zhang, T., & Wang, C. C. (2021) · Medicinal Research Reviews · doi:10.1002/med.21802 · Cited by 175
Progesterone Resistance in Endometriosis: an Acquired Property?
McKinnon, B. D., Mueller, M. D., & Montgomery, G. W. (2018) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2018.05.006 · Cited by 153
Immunological Basis of the Endometriosis: The Complement System as a Potential Therapeutic Target
Agostinis, C., Balduit, A., Mangogna, A., Zito, G., Romano, F., Ricci, G., Kishore, U., & Bulla, R. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2020.599117 · Cited by 123
Role of AMPK/mTOR, mitochondria, and ROS in the pathogenesis of endometriosis
Assaf, L., Eid, A. A., & Nassif, J. (2022) · Life Sciences · doi:10.1016/j.lfs.2022.120805 · Cited by 119
Organoids of the female reproductive tract
Chumduri, C., & Turco, M. Y. (2021) · Journal of Molecular Medicine · doi:10.1007/s00109-020-02028-0 · Cited by 110
Extracellular vesicle-associated VEGF-C promotes lymphangiogenesis and immune cells infiltration in endometriosis
Li, W.-N., Hsiao, K., Wang, C.-A., Chang, N., Hsu, P.-L., Sun, C.-H., Wu, S.-R., Wu, M., & Tsai, S. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1920037117 · Cited by 96
Inhibition of METTL3/m6A/miR126 promotes the migration and invasion of endometrial stromal cells in endometriosis
Li, X., Xiong, W., Long, X., Dai, X., Peng, Y., Xu, Y., Zhang, Z., Zhang, L., & Liu, Y. (2021) · Biology of Reproduction · doi:10.1093/biolre/ioab152 · Cited by 73
Nanomedicines for Endometriosis: Lessons Learned from Cancer Research
Moses, A. S., Demessie, A. A., Taratula, O. R., Korzun, T., Slayden, O. D., & Taratula, O. (2021) · Small · doi:10.1002/smll.202004975 · Cited by 67
Expression of programmed death-1 (PD-1) and its ligand PD-L1 is upregulated in endometriosis and promoted by 17beta-estradiol
Wu, L., Lv, C., Su, Y.-F., Li, C., Zhang, H., Zhao, X., & Li, M. (2018) · Gynecological Endocrinology · doi:10.1080/09513590.2018.1519787 · Cited by 60
The known, the unknown and the future of the pathophysiology of endometriosis
Ochoa Bernal, M. A., & Fazleabas, A. T. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25115815 · Cited by 59
“The lymphatic dissemination theory has been proposed to explain the observations of endometrial tissue moving through the vasculature and lymph nodes [30].”
Background
Altered Immunity in Endometriosis: What Came First?
Králíčková, M., Fiala, L., Lošan, P., Tomeš, P., & Větvička, V. (2018) · Immunological Investigations · doi:10.1080/08820139.2018.1467926 · Cited by 54
Endometriosis and Cancer: Exploring the Role of Macrophages
Artemova, D. A., Vishnyakova, P., Khashchenko, K. E. P., Elchaninov, A. V., Sukhikh, G. T., & Fatkhudinov, T. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22105196 · Cited by 53
Pathophysiologic processes have an impact on the plasma metabolomic signature of endometriosis patients
Vicente-Muñoz, S., Morcillo, I., Puchades‐Carrasco, L., Payá, V., Pellicer, A., & Pineda‐Lucena, A. (2016) · Fertility and Sterility · doi:10.1016/j.fertnstert.2016.09.014 · Cited by 47
The gut microbiota: a double-edged sword in endometriosis
Talwar, C., Singh, V., & Kommagani, R. (2022) · Biology of Reproduction · doi:10.1093/biolre/ioac147 · Cited by 48
Définition, description, formes anatomo-cliniques, pathogenèse et histoire naturelle de l’endométriose, RPC Endométriose CNGOF-HAS
Borghese, B., Santulli, P., Marcellin, L., & Chapron, C. (2018) · Gynécologie Obstétrique Fertilité & Sénologie · doi:10.1016/j.gofs.2018.02.017 · Cited by 47
Biological characteristics of endometriotic mesenchymal stem cells isolated from ectopic lesions of patients with endometriosis
Liu, Y., Liang, S., Yang, F., Sun, Y., Niu, L., Ren, Y., Wang, H., He, Y., Du, J., Yang, J., et al. (2020) · Stem Cell Research & Therapy · doi:10.1186/s13287-020-01856-8 · Cited by 41
Progesterone resistance in endometriosis: A pathophysiological perspective and potential treatment alternatives
Tang, H., Lin, T., Wu, M., & Tsai, S. (2024) · Reproductive Medicine and Biology · doi:10.1002/rmb2.12588 · Cited by 42
Endometriosis and inflammatory immune responses: Indian experience
Gajbhiye, R. (2022) · American Journal of Reproductive Immunology · doi:10.1111/aji.13590 · Cited by 37
Pathogenesis of bowel endometriosis
Yong, P. J., Bedaiwy, M. A., Alotaibi, F. T., & Anglesio, M. S. (2020) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2020.05.009 · Cited by 35
Application of serum markers in diagnosis and staging of ovarian endometriosis
Tang, T., Lai, H., Huang, X., Gu, L., & Shi, H. (2021) · Journal of obstetrics and gynaecology research · doi:10.1111/jog.14654 · Cited by 31
Endometriosis origin from primordial germ cells
Makiyan, Z. (2017) · Organogenesis · doi:10.1080/15476278.2017.1323162 · Cited by 31
“Lymphatic and vascular dissemination theories have been proposed to explain the presence of endometrial lesions in lymphatic vessels and the spread to lymph nodes and rare sites.(16) Immune dysfunction and deficiency impair the survival of endometrial cells and lesion establishment, and high reoccurrence rates occur f…”
Background
Lymphatic Function and Dysfunction in the Context of Sex Differences
Trincot, C. E., & Caron, K. M. (2019) · ACS Pharmacology & Translational Science · doi:10.1021/acsptsci.9b00051 · Cited by 33
Research advances in drug therapy of endometriosis
Shi, J., Tan, X., Feng, G., Yuan, Z., Jiang, Z., Banda, S., Wang, L., Zheng, W., Chen, L., Yu, D., et al. (2023) · Frontiers in Pharmacology · doi:10.3389/fphar.2023.1199010 · Cited by 30
Lymphangiogenesis induced by vascular endothelial growth factor receptor 1 signaling contributes to the progression of endometriosis in mice
Hattori, K., Ito, Y., Honda, M., Sekiguchi, K., Hosono, K., Shibuya, M., Unno, N., & Majima, M. (2020) · Journal of Pharmacological Sciences · doi:10.1016/j.jphs.2020.05.003 · Cited by 26
New World and Old World Monkeys
Mätz‐Rensing, K., Fernandes, N. C. C. D. A., & Lowenstine, L. J. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-805306-5.00014-6 · Cited by 23
Angiogenesis, Lymphangiogenesis, and the Immune Response in South African Preeclamptic Women Receiving HAART
Naicker, T., Phoswa, W. N., Onyangunga, O. A., Gathiram, P., & Moodley, J. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20153728 · Cited by 21
Small Bowel Obstruction Caused by Ileal Endometriosis with Appendiceal and Lymph Node Involvement Treated with Single-Incision Laparoscopic Surgery: A Case Report and Review of the Literature
Koyama, R., Aiyama, T., Yokoyama, R., & Nakano, S. (2021) · American Journal of Case Reports · doi:10.12659/ajcr.930141 · Cited by 19
“Emerging evidence suggests that the lymphatic system is deeply involved in the pathogenesis and progression of endometriosis [11].”
Background
Increased Angiogenesis and Lymphangiogenesis in Adenomyosis Visualized by Multiplex Immunohistochemistry
Harmsen, M. J., Arduç, A., Bleeker, M. C. G., Juffermans, L. J. M., Griffioen, A. W., Jordanova, E. S., & Huirne, J. A. F. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23158434 · Cited by 19
Distinct molecular targets of ProEGCG from EGCG and superior inhibition of angiogenesis signaling pathways for treatment of endometriosis
Hung, S. W., Gaetani, M., Li, Y., Tan, Z., Xu, Z., Zhang, R., Ding, Y., Man, G. C. W., Zhang, T., Song, Y., et al. (2023) · Journal of Pharmaceutical Analysis · doi:10.1016/j.jpha.2023.09.005 · Cited by 18
“Similarly, these endometrial cells can also circulate to ectopic sites via vascular dissemination [6].”
Background
Digestive system deep infiltrating endometriosis: What do we know
Yin, W., Li, X., Liu, P., Li, Y., Liu, J., Yu, S., & Tai, S. (2023) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.17921 · Cited by 17
“60 Other lymphangiogenic factors were also found in DIE lesions, such as VEGF-A, VEGFR-2.”
BackgroundResultInfluential
Emerging strategies for the treatment of endometriosis
Chen, Q., Wang, J., Ding, X., Zhang, Q., & Duan, P. (2024) · Biomedical Technology · doi:10.1016/j.bmt.2024.08.002 · Cited by 18
Identification of endometriosis-associated genes and pathways based on bioinformatic analysis
Wang, T., Jiang, R., Yao, Y., Qian, L., Zhao, Y. F., & Huang, X. (2021) · Medicine · doi:10.1097/md.0000000000026530 · Cited by 16
Endometriosis in para-aortic lymph node resembling a malignancy: a case report and literature review
Li, J., Liu, Y., Du, K., Xiao, L., He, X., Dai, F., & Tang, J. (2022) · BMC Women s Health · doi:10.1186/s12905-022-01659-4 · Cited by 15
“Additionally, EMs causes lymph node immune response deficiency and insufficient clearance of endometrial cells, resulting in EMs metastasis [16].”
Background
Microbiota insights in endometriosis
Parpex, G., Nicco, C., Chassaing, B., Santulli, P., Chouzenoux, S., Bourdon, M., Maignien, C., Doridot, L., Batteux, F., Chapron, C., et al. (2025) · Microbiome · doi:10.1186/s40168-025-02243-2 · Cited by 13
Promotion of BST2 expression by the transcription factor IRF6 affects the progression of endometriosis
Li, J., He, Y., Qu, Y., Ren, C.-C., Wang, X., Cheng, Y., Sun, L., Zhang, X., & Zhang, G. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1115504 · Cited by 11
The Critical Role of Host and Bacterial Extracellular Vesicles in Endometriosis
Wagner, M., Hicks, C., El-Omar, E. M., Combes, V., & El‐Assaad, F. (2024) · Biomedicines · doi:10.3390/biomedicines12112585 · Cited by 11
Juan-tong-yin potentially impacts endometriosis pathophysiology by enhancing autophagy of endometrial stromal cells via unfolded protein reaction-triggered endoplasmic reticulum stress
Meng, F., Li, J., Dong, K., Bai, R., Liu, Q., Lu, S., Liu, Y., Wu, D., Jiang, C., & Li, W. (2024) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2024.117859 · Cited by 9
Circ_0001495 influences the development of endometriosis through the miRNA-34c-5p/E2F3 axis
Yue, Y., Lu, B., & Ni, G. (2024) · Reproductive Biology · doi:10.1016/j.repbio.2024.100876 · Cited by 9
Primary Retroperitoneal Carcinomas: New Insights into Pathogenesis and Clinical Management in Comparison with Ovarian Carcinomas and Carcinoma of Unknown Primary
Otsuka, I. (2023) · Cancers · doi:10.3390/cancers15184614 · Cited by 9
“Endometriosis is believed to disseminate via the lymphatic system [141].”
Background
Actual research trends in etiology and pathogenesis of endometriosis (a review)
Владимировна, С. А., Gunin, A. G., Sidorov, A. Е., Denisova, T., Chernyshov, V. V., & Smirnova, T. L. (2020) · Russian Journal of Human Reproduction · doi:10.17116/repro202026051118 · Cited by 9
Evidence for lymphatic pathogenesis of endosalpingiosis: the more things change, the more they stay the same
Russell, P., & Anderson, L. A. (2015) · Pathology · doi:10.1016/j.pathol.2015.11.024 · Cited by 9
The causality between gut microbiota and endometriosis: a bidirectional Mendelian randomization study
Yang, H. (2024) · Frontiers in Medicine · doi:10.3389/fmed.2024.1434582 · Cited by 8
Biomarkers of endometriosis
Arsalan, H. M., Mumtaz, H., & Laganà, A. S. (2025) · Advances in clinical chemistry · doi:10.1016/bs.acc.2025.01.004 · Cited by 10
Therapeutic effects of melatonin on endometriosis, targeting molecular pathways: Current knowledge and future perspective
Sharifi, M., Nikoo, N. R., Badehnoosh, B., Shafabakhsh, R., Asemi, R., Reiter, R. J., & Asemi, Z. (2023) · Pathology - Research and Practice · doi:10.1016/j.prp.2023.154368 · Cited by 8
RETRACTED: Dye diffusion during laparoscopic tubal patency tests may suggest a lymphatic contribution to dissemination in endometriosis: A prospective, observational study
Scioscia, M., Pesci, A., Scardapane, A., Noventa, M., Bonaccorsi, G., Greco, P., & Zamboni, G. (2019) · PLoS ONE · doi:10.1371/journal.pone.0226264 · Cited by 8
“Different studies assessed biochemical (growth factors and cytokines) and histological features during menstrual changes in lymphatics in eutopic and heterotopic endometrial tissues as summarized by Jerman and Hey-Cunningham [16].”
Influential
Retracted
Endometriosis of para-aortic node masquerading a malignancy: a rare occurrence
Christable, E., Shivkumaran, S., Venkitaraman, B., & Kajamohideen, S. (2021) · BMJ Case Reports · doi:10.1136/bcr-2020-240750 · Cited by 8
Indocyanine green-guided sentinel lymph node mapping during laparoscopic surgery with vaginal cuff closure but no uterine manipulator for cervical cancer
Aoki, Y., Kanao, H., Fusegi, A., Omi, M., Okamoto, S., Tanigawa, T., Nomura, H., Omatsu, K., & Tonooka, A. (2022) · International Journal of Clinical Oncology · doi:10.1007/s10147-022-02197-7 · Cited by 8
“Deep infiltrating endometriosis has been observed in patients for whom frozen sectioning yielded a false-negative diagnosis [14], suggesting that endometriosis may affect lymphatic vessels [35].”
Background
Rationally-designed Chitosan-based Polymeric Nanomaterials According to Intrinsic Characteristics for Cancer Therapy and Theranostics: A Review
Yu, F., Zhu, Y., Shang, X., Yuan, H., & Hu, F. (2022) · Current Medicinal Chemistry · doi:10.2174/0929867329666220620164429 · Cited by 8
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 8
Analysis of the Biopsychosocial Impacts Associated with Endometriosis to Improve Patient Care
Noditi, A., Bostan, I.-S., Scurtu, F., Ionescu, D., Mehedintu, A. M., Petca, A. T., Mehedințu, C., Bostan, M., & Rotaru, A. M. (2025) · Journal of Clinical Medicine · doi:10.3390/jcm14072158 · Cited by 9
“This phenomenon may provide a plausible explanation for the occurrence of endometriosis in these distant locations [20].”
Medical treatments of endometriosis: a review
Elbasueny, B., Geerts, M., Yang, E. C., Allaire, C., Yong, P. J., & Bedaiwy, M. A. (2022) · Reproductive and Developmental Medicine · doi:10.1097/rd9.0000000000000053 · Cited by 9
Value of indocyanine green pelvic lymph node mapping in the surgical approach of cervical cancer
Papathemelis, T., Scharl, A. J., Anapolski, M., Inwald, E. C., Ignatov, A., Ortmann, O., Gerken, M., Klinkhammer‐Schalke, M., & Scharl, S. (2020) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-020-05457-x · Cited by 7
A case of infiltrative cecal endometriosis with appendiceal obliteration and lymph node involvement
Law, Y. Y., Patel, R., Yorke, R. F., Bailey, H. R., & Eps, J. L. V. (2020) · Journal of Surgical Case Reports · doi:10.1093/jscr/rjaa396 · Cited by 6
NeiyiKangfu tablets control the progression of endometriosis through inhibiting RAF/MEK/ERK signal pathway by targeting RKIP
Wen, Y., Fan, L.-X., Pang, L., Zhao, T.-T., Li, R., Zhang, Y., Zhang, L., & Yang, W. (2022) · Gynecological Endocrinology · doi:10.1080/09513590.2022.2162495 · Cited by 6
Sox-2 positive cells identified in lymph nodes from endometriosis patients may play a role in the disease pathogenesis
Velho, R. V., Danielyan, I., Mechsner, S., & Götte, M. (2023) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2023.07.017 · Cited by 7
Role of computed tomography in imaging of endometriosis
Ghosh, S., Alhamshari, A., Prajapati, P., Nakrour, N., Carnelli, C., Kilcoyne, A., Harisinghani, M. G., Tsai, L. L., Catalano, O. A., Kambadakone, A. R., et al. (2025) · Abdominal Radiology · doi:10.1007/s00261-025-04907-x · Cited by 8
Association between tumor necrosis factor-α gene-1031T/C promoter polymorphism and endometriosis in a European population
Drakou, A., Mavrogianni, D., Ntzeros, K., Πρωτόπαπας, Α., Drakakis, P., & Loutradis, D. (2019) · Hormone Molecular Biology and Clinical Investigation · doi:10.1515/hmbci-2019-0033 · Cited by 5
Treatment of endometriosis with mifepristone mediated by nanostructured lipid carriers
Yan, J., Peng, Y., Huang, S., Fei, W., Chen, Y., Zheng, C., Zhang, M., & Zhao, M. (2024) · Drug Delivery and Translational Research · doi:10.1007/s13346-024-01661-3 · Cited by 4
Endometriosis Stem Cell Sources and Potential Therapeutic Targets: Literature Review and Bioinformatics Analysis
Jin, Z., Zhang, Y., Li, J., Lv, S., Zhang, L., & Feng, Y. (2021) · Regenerative Medicine · doi:10.2217/rme-2021-0039 · Cited by 4
Thoracic Endometriosis: A Presentation of an Uncommon Disease in a Black African Woman
Ogunkoya, J. O., Solaja, T. O., Ogunlade, A. F., & Ogunmola, M. I. (2022) · Case Reports in Medicine · doi:10.1155/2022/2380700 · Cited by 5
Deep infiltrating endometriosis mimicking colorectal cancer
Wu, C., Wei, M. Y.-K., Yeung, J. M. C., Battye, S., & Cho, J. Y. (2023) · ANZ Journal of Surgery · doi:10.1111/ans.18525 · Cited by 4
Gut Microbiota, Circulating Metabolites and Risk of Endometriosis: A Two-Step Mendelian Randomization Study
Yang, H. (2024) · Polish Journal of Microbiology · doi:10.33073/pjm-2024-041 · Cited by 3
“…including the concepts of abnormal remnants of embryonic Müllerian ducts (Lambrinoudaki et al. 2009), coelomic metaplasia (Vercellini et al. 2014), metastatic spread via vascular or lymphatic vessels (Jerman and Hey-Cunningham 2015), and determinism of the eutopic endometrium (Maia et al. 2012).”
Exploring endometriosis through 3D in vitro models: A narrative review
Juli, C., Nyang’au, E. M., Götte, M., & von Versen‐Höynck, F. (2026) · Materials Today Bio · doi:10.1016/j.mtbio.2026.103032 · Cited by 3
“Endometriotic cells may also be distributed to ectopic sites via lymphovascular metastasis [5].”
Splenic lesion mimicking breast metastasis: The first description of splenic parenchymal endometriosis
Weyl, A., Illac, C., Delchier, M.-C., Suc, B., Cuellar, E., & Chantalat, É. (2020) · Journal of Endometriosis and Pelvic Pain Disorders · doi:10.1177/2284026520960846 · Cited by 3
The Genetic-Epigenetic Pathophysiology of Endometriosis: A Surgeon’s View
Koninckx, P. R., Ussia, A., Adamyan, L. V., Keckstein, J., Wattiez, A., Gomel, V., & Martin, D. C. (2020) · Springer eBooks · doi:10.1007/978-3-030-52984-0_6 · Cited by 3
Osteopontin as a marker of endometriosis — the current state of knowledge
Figuła, J., Baran, R. M., & Jach, R. (2023) · Ginekologia Polska · doi:10.5603/gpl.86232 · Cited by 3
“These include: Samp-son’s implantation theory [13], the theory of the spread of endometrial cells through the lymphatic and circulatory systems [14] or the Meyer’s theory of metaplasia [15].”
Tissue and molecular effects of the cavitated solution in the endometrial receptivity rehabilitation of patients with the uterine infertility
Мелкозерова, О. А., Башмакова, Н. В., Chistyakova, G. N., Esareva, A. V., Barlit, O. G., & Giniyatova, A. A. (2017) · Russian Journal of Human Reproduction · doi:10.17116/repro201723573-83 · Cited by 3
Multifocal endometriosis
Lozneanu, L., Ciobanu-Apostol, D. G., Balan, R. A., Păvăleanu, I., Giuşcă, S. E., Căruntu, I.-D., & Amălinei, C. (2016) · Archive of Clinical Cases · doi:10.22551/2016.12.0303.10078 · Cited by 3
Endometriosis and the Hallmarks of Cancer
Ellis, K. B., & Wood, R. (2025) · Reproductive Sciences · doi:10.1007/s43032-025-02024-0 · Cited by 3
Endometriosis
Hays, B. M., & Hudson, T. (2020) · Elsevier eBooks · doi:10.1016/b978-0-323-43044-9.00166-7 · Cited by 2
Endometriosis lesions are oligoclonal structures derived from the normal endometriumPreprint
Ólafsson, S., Arnthorsson, A. O., Kübler, K., Sigurðsson, Á., Gunnarsdottir, H. S., Jónsson, H., Ásbjörnsdóttir, B., le Roux, L., Saemundsdottir, J., Steinthórsdóttir, V., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.02.25.708037 · Cited by 3
“…the stem cell recruitment theory states that endometriosis lesions originate from stem cells travelling through the angiolymphatic circulation ( 10 ), but opinions are divided as to whether these stem cells would be of uterine origin or derived from other stem-cell niches, in particular the…”
Medikamentozno zdravljenje endometrioze: pregled stanja in nove možnosti zdravljenja
Jakič, M., Vogler, A., & Rižner, T. L. (2016) · Slovenian Medical Journal · doi:10.6016/zdravvestn.1416 · Cited by 1
CURRENT PERSPECTIVES OF MODERN AND TRADITIONAL MEDICATIONS OF LIFESTYLE GYNECOLOGIC DISORDERS: A REVIEW
(2022) · International Journal of Biology Pharmacy and Allied Sciences · doi:10.31032/ijbpas/2022/11.6.6172 · Cited by 1
A seed or soil problem in early endometriosis: stromal cell origin drives cellular invasion and coupling over mesothelial cell origin
Go, V.-A. A., Chavez, J. B., Robinson, R. D., & Nicholson, B. J. (2024) · F&S Science · doi:10.1016/j.xfss.2024.08.001 · Cited by 1
Identification of hub biomarkers and immune cell infiltrations participating in the pathogenesis of endometriosis
Li, K., Wang, J., Liu, X., Dang, Y., Wang, K., Li, M., Zhang, X., & Liu, Y. (2025) · Scientific Reports · doi:10.1038/s41598-025-86164-y · Cited by 2
Endometrioma: A Comprehensive Review of Its Varied Presentations, Complications, and Impact on Patient Management
Ghosh, S., Mann, K., Nakrour, N., Ray, L. J., Movilla, P. R., Harisinghani, M. G., Kambadakone, A., & Shenoy‐Bhangle, A. S. (2025) · Journal of Gastrointestinal and Abdominal Radiology · doi:10.1055/s-0045-1809315 · Cited by 2
“12 The ovary is the most common site of ectopic endo-metriotic implantation.”
Dynamics of Conventional Metabolic Indices in Relation to Endometriosis Severity: A Retrospective Analysis
Zhong, X., Lu, W., Zhang, Q., Dong, J., Xiao, H., & Tu, R. (2025) · International Journal of General Medicine · doi:10.2147/ijgm.s537848 · Cited by 1
“7 10 Deep endometriotic lesions have the potential to infiltrate nerves 11 and lymph nodes, 12 causing heightened negative effects on the body.”
The mental health burden of endometriosis: a narrative review
Servidoni, A. C. P., Surmann, H., Canis, M. J., Taylor, H. S., Crippa, J. A., & Abrão, M. S. (2026) · F&S Reviews · doi:10.1016/j.xfnr.2026.100109 · Cited by 2
An unusual clinical presentation and histological findings provide insight into the pathogenesis of endometriosis
Simpson, P., Tyler, X., & Morris, E. (2016) · Gynecological Surgery · doi:10.1007/s10397-016-0984-y · Cited by 1
“This was also shown in the comprehensive review Jerman in 2015 [8], which highlighted that whilst endometrial tissue can be found in both pelvic and paraaortic lymph nodes, it is quite rare and when it does occur it is usually glandular inclusions consistent with endometriosis rather than formed endometriotic cysts.”
Background
Endometriosis umbilical primaria. Reporte de dos casos
Álvarez, A. T., Carrasco, A. L., Velacoracho-Pérez, J. J., Zarbakhsh-Etemadi, S., Yébenes-Gregorio, L., Hardisson-Hernaez, D., & Hernández, A. (2022) · Revista chilena de obstetricia y ginecología · doi:10.24875/rechog.m21000037 · Cited by 1
Prominent Pseudo-Angiovascular invasion by benign gallbladder epithelium and bile emboli in a patient with delayed cholecystectomy due to COVID-19 positive test
Miller, Q., Dave, N., Popnikolov, N. K., Bruce, S. D., & Mesa, H. A. (2022) · Surgical and Experimental Pathology · doi:10.1186/s42047-022-00120-y · Cited by 1
“…to medical intervention, in the context of benign processes, has been described in benign proliferative processes of the breast (Eusebai and Azzopardi 1976), endometriosis (Jerman and Hey-Cunningham 2015), endosalpingiosis (Russell and Anderson 2016) and vasitis nodosa (Balogh and Travis 1985).”
Background
Endometriosis-induced acute large bowel obstruction and endometriotic deposits in pericolic lymph nodes: A case report
Hamdy, O., Ragab, D., Farouk, B., Allam, M. M., Asy, R. A., Elemam, N. M., Saleh, G. A., & Ghorab, D. S. (2025) · Journal of Endometriosis and Pelvic Pain Disorders · doi:10.1177/22840265251341420 · Cited by 1
The Efficiency of Intrauterine Irrigation of the Cavitated Drug Solutes in Patients with Endometrial Receptivity Disorders
Melkozerova, O. A. (2018) · Journal of Gynecology and Obstetrics · doi:10.11648/j.jgo.20180604.15 · Cited by 1
Endometrial Immune-Inflammatory Gene Signatures in Endometriosis
Miller, J. E., Symons, L. K., Marks, R. M., & Tayade, C. (2019) · Springer eBooks · doi:10.1007/978-3-030-28584-5_10 · Cited by 1
Transcoelomic and Lympho-Hematogenous Dissemination of Endometrioid Heterotopias – the Mechanism of Extragenital Endometriosis Formation
Ukrainets, R. V., & Korneva, Y. S. (2021) · Journal of Anatomy and Histopathology · doi:10.18499/2225-7357-2021-10-1-85-91 · Cited by 1
Endometriosis impact on the course of pregnancy and obstetric outcomes
Жабіцька, Л. А., & Жабіцька, Л. А. (2021) · Reproductive Endocrinology · doi:10.18370/2309-4117.2021.60.31-33 · Cited by 1
Afectación ganglionar en endometriosis rectal aislada
Fernández-Val, J. F., García-González, J. M., del Tánago, J. G., & Colina-Alonso, A. (2015) · Medicina Clínica · doi:10.1016/j.medcli.2015.04.026
Lymph node involvement in isolated rectal endometriosis
Fernández-Val, J. F., García-González, J. M., del Tánago, J. G., & Colina-Alonso, A. (2016) · Medicina Clínica (English Edition) · doi:10.1016/j.medcle.2015.04.010
MRT der Endometriose und Adenomyose
Ertmer, A., Grabherr, R., & Huch, R. (2019) · Radiologie up2date · doi:10.1055/a-0970-9646
“Bei dieser Unterform wird eine metastatische Aussaat in regionale Lymphknoten beschrieben, insbesondere bei tiefer Infiltration des Darms [2, 14,21,25,26].”
BackgroundInfluential
Hypoxia and immune factors
Li, W., Wu, M. H., & Tsai, S. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-820661-4.00021-2
Pathogenesis and Pathophysiology of the Effect of Endometriosis on Reproductive Function
Zhabitskaya, L. A., & Guzhevskaya, I. V. (2022) · Репродуктивное здоровье Восточная Европа · doi:10.34883/pi.2021.11.6.010
Endometriosis Treatment
Wu, C. Z., Klebanoff, J. S., & Moawad, G. (2020) · Wiley eBooks · doi:10.1002/9781119482598.ch34

Authors: Jerman, L. F., & Hey-Cunningham, A. J.
Affiliations: The University of Sydney (AU)
Corresponding author: Jerman, Laila F.
Venue: Biology of Reproduction
Publisher: Oxford University Press (OUP)
Published: 2015-03-01
Volume: 92
Issue: 3
Pages: 64-64
ISSN: 0006-3363 (ISSN-L)
1529-7268
DOI: 10.1095/biolreprod.114.124313
OpenAlex: W2152401059
Cited by: 122
References: 153
Citations by year: 2026: 13 · 2025: 13 · 2024: 13 · 2023: 12 · 2022: 16 · 2021: 14 · 2020: 14 · 2019: 9 · 2018: 7 · 2017: 4 · 2016: 5 · 2015: 2
FWCI: 0.91
Type: journal article
Language: en
Open access: closed
Locations: Biology of Reproduction (publishedVersion)
PubMed (publishedVersion)
BioOne Complete (BioOne) (submittedVersion)
Topics: Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
Health Sciences › Medicine › Obstetrics and Gynecology › Gynecological conditions and treatments
Health Sciences › Medicine › Infectious Diseases › Diagnosis and treatment of tuberculosis
Keywords: endometriosis, lymphatic system, lymphangiogenesis, lymphatic vessel density, pelvic lymph nodes, endometriotic lesions, immune response, endometriosis pathogenesis, endometriosis recurrence, eutopic endometrium
MeSH terms: Animals, Disease Models, Animal, Endometriosis, Endometrium, Female, Humans, Lymphatic System, Pelvis, Uterus, Disease Progression

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

The Role of the Lymphatic System in Endometriosis: A Comprehensive Review of the Literature1

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks