The Role of the Lymphatic System in Endometriosis: A Comprehensive Review of the Literature1
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
Cites
Statistics
Claims the paper makes
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?
In most bowel lesions, lymph nodes are invaded.
“In most bowel lesions lymph nodes are invaded (17,18).”
From Pathogenesis of deep endometriosis (2017) · cites this paper as [18]
Cites
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 · see citing works
Giudice, L. C., & Kao, L. C. (2004) · The Lancet · doi:10.1016/s0140-6736(04)17403-5 · Cited by 3,166 · see citing works
Sampson, J. A. (1927) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(15)30003-x · Cited by 2,334 · see citing works
Nisolle, M., & Donnez, J. (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)00191-x · Cited by 1,279 · see citing works
(1927) · PubMed Central · Cited by 1,008 · see citing works
(1984) · PubMed · Cited by 997 · see citing works
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 · see citing works
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 · see citing works
Recurrence of endometriosis and its control
Guo, S.-W. (2009) · Human Reproduction Update · doi:10.1093/humupd/dmp007 · Cited by 719 · see citing works
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 · see citing works
Kahn, H. J., Bailey, D. J., & Marks, A. (2002) · Modern Pathology · doi:10.1038/modpathol.3880543 · Cited by 601 · see citing works
Aromatase expression in endometriosis.
Noble, L. S., Simpson, E. R., Johns, A., & Bulun, S. E. (1996) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.81.1.8550748 · Cited by 566 · see citing works
Normal Structure, Function, and Histology of Lymph Nodes
Willard-Mack, C. L. (2006) · Toxicologic Pathology · doi:10.1080/01926230600867727 · Cited by 540 · see citing works
Vascular endothelial growth factor (VEGF) in endometriosis
Donnez, J., Smoes, P., Gillerot, S., Casanas-Roux, F., & Nisolle, M. (1998) · Human Reproduction · doi:10.1093/humrep/13.6.1686 · Cited by 531 · see citing works
McLaren, J. F., Prentice, A., Jones, D. S., Millican, S. A., Müller, K. H., Sharkey, A., & Smith, S. K. (1996) · Journal of Clinical Investigation · doi:10.1172/jci118815 · Cited by 499 · see citing works
Cavaillon, J. (1994) · Biomedicine & Pharmacotherapy · doi:10.1016/0753-3322(94)90005-1 · Cited by 453 · see citing works
Vascular Endothelial Growth Factor Receptor-3 in Lymphangiogenesis in Wound Healing
Paavonen, K., Puolakkainen, P. A., Jussila, L., Jahkola, T., & Alitalo, K. K. (2000) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)65021-3 · Cited by 395 · see citing works
Burke, T. W., Levenback, C., Tornos, C. S., Morris, M., Wharton, J. T., & Gershenson, D. M. (1996) · Gynecologic Oncology · doi:10.1006/gyno.1996.0211 · Cited by 364 · see citing works
Blocking Neuropilin-2 Function Inhibits Tumor Cell Metastasis
Caunt, M., Mak, J., Liang, W., Stawicki, S. S., Pan, Q., Tong, R. K., Kowalski, J., Ho, C., Reslan, H. B., Ross, J., et al. (2008) · Cancer Cell · doi:10.1016/j.ccr.2008.01.029 · Cited by 342 · see citing works
Incidence and risk of arm oedema following treatment for breast cancer: a three-year follow-up study
Clark, B., Sitzia, J., & Harlow, W. (2005) · QJM · doi:10.1093/qjmed/hci053 · Cited by 339 · see citing works
Neuropilin-2 mediates VEGF-C–induced lymphatic sprouting together with VEGFR3
Xu, Y., Yuan, L., Mak, J., Pardanaud, L., Caunt, M., Kasman, I. M., Larrivée, B., Toro, R. D., Suchting, S., Medvinsky, A., et al. (2010) · The Journal of Cell Biology · doi:10.1083/jcb.200903137 · Cited by 339 · see citing works
Basal and stimulated secretion of cytokines by peritoneal macrophages in women with endometriosis
Rana, N., Braun, D. P., House, R., Gebel, H., Rotman, C., & Dmowski, W. P. (1996) · Fertility and Sterility · doi:10.1016/s0015-0282(16)58262-4 · Cited by 264 · see citing works
Insulin-like growth factors 1 and 2 induce lymphangiogenesis in vivo
Björndahl, M. A., Cao, R., Nissen, L. J., Clasper, S., Johnson, L. A., Xue, Y., Zhou, Z., Jackson, D. G., Hansen, A. J., & Cao, Y. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0507865102 · Cited by 249 · see citing works
Potential involvement of the immune system in the development of endometriosis
Kyama, C. M., Debrock, S., Mwenda, J. M., & D'Hooghe, T. M. (2003) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-1-123 · Cited by 244 · see citing works
Estrogen Receptor-β, Estrogen Receptor-α, and Progesterone Resistance in Endometriosis
Bulun, S., Cheng, Y.-H., Pavone, M., Xue, Q., Attar, E., Trukhacheva, E., Tokunaga, H., Utsunomiya, H., Yin, P., Luo, X., et al. (2010) · Seminars in Reproductive Medicine · doi:10.1055/s-0029-1242991 · Cited by 243 · 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
Endometriosis, retrograde menstruation and peritoneal inflammation in women and in baboons
D'Hooghe, T. M. (2002) · Human Reproduction Update · doi:10.1093/humupd/8.1.84 · Cited by 231 · see citing works
Spontaneous Apoptosis of Endometrial Tissue is Impaired in Women with Endometriosis
Gebel, H. M., Braun, D. P., Tambur, A. R., Frame, D. G., Rana, N., & Dmowski, W. P. (1998) · Fertility and Sterility · doi:10.1016/s0015-0282(98)00073-9 · Cited by 228 · see citing works
Dmowski, W. P., & Braun, D. P. (2004) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2004.02.001 · Cited by 225 · see citing works
Reproductive Biology and Endocrinology – Choose an exciting venture for the scientific future
Bukovský, A. (2003) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-1-1 · Cited by 218 · see citing works
Cytokine secretion in macrophages and other cells: Pathways and mediators
Stow, J. L., Low, P. C., Offenhäuser, C., & Sangermani, D. (2009) · Immunobiology · doi:10.1016/j.imbio.2008.11.005 · Cited by 205 · see citing works
Macrophage expression in endometrium of women with and without endometriosis
Berbic, M., Schulke, L., Markham, R., Tokushige, N., Russell, P. J., & Fraser, I. S. (2008) · Human Reproduction · doi:10.1093/humrep/den393 · Cited by 204 · see citing works
Inhibition of the mammalian target of rapamycin impedes lymphangiogenesis
Huber, S. L., Bruns, C. J., Schmid, G., Hermann, P. C., Conrad, C. H., Niess, H., Huss, R., Graeb, C., Jauch, K. ‐., Heeschen, C., et al. (2007) · Kidney International · doi:10.1038/sj.ki.5002112 · Cited by 203 · see citing works
The peritoneal environment in endometriosis
Oral, E. (1996) · Human Reproduction Update · doi:10.1093/humupd/2.5.385 · Cited by 201 · see citing works
Hormone and growth factor signaling in endometrial renewal: Role of stem/progenitor cells
Gargett, C. E., Chan, R., & Schwab, K. E. (2008) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2008.02.026 · Cited by 192 · see citing works
Бурлев, В. А., Volkov, N. I., Pavlovitch, S. V., Lets, N., Larsson, A. O., & Olovsson, M. (2006) · Reproduction · doi:10.1530/rep.1.01110 · Cited by 192 · see citing works
Bergqvist, A., Bruse, C., Carlberg, M., & Carlström, K. (2001) · Fertility and Sterility · doi:10.1016/s0015-0282(00)01752-0 · Cited by 190 · 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
Kaldjian, E. P., Gretz, J. E., Anderson, A. O., Shi, Y., & Shaw, S. (2001) · International Immunology · doi:10.1093/intimm/13.10.1243 · Cited by 185 · see citing works
Dendritic cell populations in the eutopic and ectopic endometrium of women with endometriosis
Schulke, L., Berbic, M., Manconi, F., Tokushige, N., Markham, R., & Fraser, I. S. (2009) · Human Reproduction · doi:10.1093/humrep/dep071 · 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
Molecular Network Analysis of Endometriosis Reveals a Role for c-Jun–Regulated Macrophage Activation
Beste, M. T., Pfäffle-Doyle, N., Prentice, E. A., Morris, S., Lauffenburger, D. A., Isaacson, K., & Griffith, L. G. (2014) · Science Translational Medicine · doi:10.1126/scitranslmed.3007988 · Cited by 166 · see citing works
Angiogenesis and Endometriosis
Rocha, A. L. L., dos Reis, F. M., & Taylor, R. N. (2013) · Obstetrics and Gynecology International · doi:10.1155/2013/859619 · Cited by 162 · see citing works
Differential macrophage infiltration in early and advanced endometriosis and adjacent peritoneum
Khan, K. N., Masuzaki, H., Fujishita, A., Kitajima, M., Sekine, I., & Ishimaru, T. (2004) · Fertility and Sterility · doi:10.1016/j.fertnstert.2003.07.037 · Cited by 161 · see citing works
Berbic, M., Hey‐Cunningham, A. J., Ng, C. H. M., Tokushige, N., Ganewatta, S. P., Markham, R., Russell, P. J., & Fraser, I. S. (2010) · Human Reproduction · doi:10.1093/humrep/deq020 · Cited by 158 · see citing works
Ford, J., English, J., Miles, W. F. A., & Giannopoulos, T. (2004) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.2004.00093.x · Cited by 157 · see citing works
A comparative study of the in vitro antioxidant activity of statins
Franzoni, F., Quiñones-Galvan, A., Regoli, F., Ferrannini, E., & Galetta, F. (2003) · International Journal of Cardiology · doi:10.1016/s0167-5273(02)00577-6 · Cited by 156 · see citing works
Antsiferova, Y. S., Sotnikova, N. Y., Посисеева, Л. В., & Shor, A. L. (2005) · Fertility and Sterility · doi:10.1016/j.fertnstert.2005.05.066 · Cited by 155 · see citing works
Cell proliferation is increased in the endometrium of women with endometriosis
Wingfield, M. B., Macpherson, A., Healy, D. L., & Rogers, P. A. W. (1995) · Fertility and Sterility · doi:10.1016/s0015-0282(16)57733-4 · Cited by 155 · see citing works
Al-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
Javert, C. T. (1949) · Cancer · doi:10.1002/1097-0142(194905)2:3 · Cited by 150 · see citing works
Gargett, C. E., Chan, R., & Schwab, K. E. (2007) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/gco.0b013e328235a5c6 · Cited by 141 · see citing works
Macrophages and nerve fibres in peritoneal endometriosis
Tran, L. V. P., Tokushige, N., Berbic, M., Markham, R., & Fraser, I. S. (2008) · Human Reproduction · doi:10.1093/humrep/den483 · Cited by 138 · see citing works
Regulatory T cells and other leukocytes in the pathogenesis of endometriosis
Berbic, M., & Fraser, I. S. (2011) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2010.11.004 · Cited by 135 · see citing works
Olkowska-Truchanowicz, J., Bocian, K., Maksym, R. B., Bialoszewska, A., Wlodarczyk, D., Baranowski, W., Zabek, J., Korczak-Kowalska, G., & Malejczyk, J. (2013) · Human Reproduction · doi:10.1093/humrep/des346 · Cited by 131 · see citing works
Supriyadi, E., Veerman, A. J. P., Sutaryo, S., Purwanto, I., van de Ven, P. M., & Cloos, J. J. (2012) · Journal of Oncology · doi:10.1155/2012/135186 · Cited by 128 · 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
Structure and Function of Lymphatics
Ryan, T. J. (1989) · Journal of Investigative Dermatology · doi:10.1038/jid.1989.4 · Cited by 127 · see citing works
Gilabert–Estellés, J., Ramón, L., España, F., Gilabert, J., Vila, V., Regañón, E., Castelló, R., Chirivella, M., & Estellés, A. (2007) · Human Reproduction · doi:10.1093/humrep/dem149 · Cited by 126 · see citing works
Endometriosis: abnormal endometrium and dysfunctional immune response
Braun, D. P., & Dmowski, W. P. (1998) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/00001703-199810000-00003 · Cited by 123 · see citing works
Lymphatic function and immune regulation in health and disease
Liao, S., & Padera, T. P. (2013) · Lymphatic Research and Biology · doi:10.1089/lrb.2013.0012 · Cited by 122 · see citing works
A Modified Baboon Model for Endometriosis
Fazleabas, A. T., Brudney, A., Gürateş, B., Chai, D. C., & Bulun, S. E. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb02791.x · Cited by 120 · see citing works
Machado, D. E., Berardo, P. T., Palmero, C. Y., & Nasciutti, L. E. (2010) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/1756-9966-29-4 · Cited by 120 · see citing works
Routes of Lymphatic Spread: A Study of 112 Consecutive Patients with Endometrial Cancer
Mariani, A., Webb, M. J., Keeney, G. L., & Podratz, K. C. (2001) · Gynecologic Oncology · doi:10.1006/gyno.2000.6111 · Cited by 119 · see citing works
LYVE-1 immunohistochemical assessment of lymphangiogenesis in endometrial and lung cancer: Figure 1
Koukourakis, M. I., Giatromanolaki, A. N., Sivridis, E., Simopoulos, C., Gatter, K. C., Harris, A. L., & Jackson, D. G. (2005) · Journal of Clinical Pathology · doi:10.1136/jcp.2004.019174 · Cited by 119 · see citing works
Evaluation of biodistribution and safety of adenovirus vector containing MDR1 in mice
Zhao, Z., Liu, W., Su, Y., Zhu, J., Zheng, G., Luo, Q., & Jin, X. (2010) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/1756-9966-29-1 · Cited by 118 · see citing works
Lymphatic Drainage of the Peritoneal Space: A Pattern Dependent on Bowel Lymphatics
Parungo, C. P., Soybel, D. I., Colson, Y. L., Kim, S., Ohnishi, S., Grand, A. M. D., Laurence, R. G., Soltesz, E. G., Chen, F. Y., Cohn, L. H., et al. (2006) · Annals of Surgical Oncology · doi:10.1245/s10434-006-9044-6 · Cited by 117 · see citing works
Phenotypic and functional studies of leukocytes in human endometrium and endometriosis
Jones, R. K. (1998) · Human Reproduction Update · doi:10.1093/humupd/4.5.702 · Cited by 115 · see citing works
Machado, D. E., Abrão, M. S., Berardo, P. T., Takiya, C. M., & Nasciutti, L. E. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.05.076 · Cited by 112 · see citing works
Vascular endothelial growth factor A and C gene expression in endometriosis
Takehara, M., Ueda, M., Yamashita, Y., Terai, Y., Hung, Y., & Ueki, M. (2004) · Human Pathology · doi:10.1016/j.humpath.2004.07.020 · Cited by 110 · see citing works
Stem cell theory for the pathogenesis of endometriosis
Maruyama, T. (2012) · Frontiers in Bioscience · doi:10.2741/e589 · Cited by 109 · see citing works
Carr, I. (1983) · Cancer and Metastasis Reviews · doi:10.1007/bf00048483 · Cited by 109 · see citing works
Abengózar, M. Á., de Frutos, S., Ferreiro, S., Soriano, J., Pérez‐Martínez, M., Olmeda, D., Marenchino, M., Cañamero, M., Ortega, S., Megı́as, D., et al. (2012) · Blood · doi:10.1182/blood-2011-09-380006 · Cited by 108 · see citing works
Peritoneal fluid environment in endometriosis. Clinicopathological implications.
Bedaiwy, M. A., & Falcone, T. (2003) · PubMed · Cited by 108 · see citing works
Carlo, C. D., Bonifacio, M., Tommaselli, G. A., Bifulco, G., Guerra, G., & Nappi, C. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.03.079 · Cited by 104 · see citing works
Tan, X., Lang, J., Liu, D., Shen, K., Leng, J., & Zhu, L. (2002) · Fertility and Sterility · doi:10.1016/s0015-0282(02)03187-4 · Cited by 100 · see citing works
Tumor-induced lymphangiogenesis: A target for cancer therapy?
Thiele, W., & Sleeman, J. P. (2006) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2006.01.007 · Cited by 99 · see citing works
Hobbs, J. E., & BORTNICK, A. R. (1940) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(15)30807-3 · Cited by 99 · see citing works
Sleeman, J. P., Schmid, A., & Thiele, W. (2009) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2009.05.005 · Cited by 97 · see citing works
Kempuraj, D., Papadopoulou, N., Stanford, E. J., Christodoulou, S., Madhappan, B., Sant, G. R., Solage, K., Adams, T., & Theoharides, T. C. (2004) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.2004.00224.x · Cited by 94 · see citing works
Granstein, R. D., Deak, M. R., Jacques, S. L., Margolis, R. J., Flotte, T. J., Whitaker, D., Long, F. H., & Amento, E. P. (1989) · Journal of Investigative Dermatology · doi:10.1111/1523-1747.ep12277336 · Cited by 93 · see citing works
Tumor Lymphangiogenesis as a Potential Therapeutic Target
Duong, T., Koopman, P. A., & François, M. (2012) · Journal of Oncology · doi:10.1155/2012/204946 · Cited by 88 · see citing works
Pathogenesis of Endometriosis: The Role of Peritoneal Fluid
Koninckx, P. R., Kennedy, S., & Barlow, D. (1999) · Gynecologic and Obstetric Investigation · doi:10.1159/000052856 · Cited by 85 · see citing works
Catherino, W. H., Parrott, E. C., & Segars, J. H. (2010) · Fertility and Sterility · doi:10.1016/j.fertnstert.2010.08.049 · Cited by 83 · see citing works
Histologic study of endometriosis and examination of lymphatic drainage in and from the uterus
Ueki, M. (1991) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(91)90252-m · Cited by 82 · see citing works
Delbandi, A., Mahmoudi, M., Shervin, A., Akbari, E., Jeddi‐Tehrani, M., Sankian, M., Kazemnejad, S., & Zarnani, A. (2013) · Fertility and Sterility · doi:10.1016/j.fertnstert.2013.04.041 · Cited by 79 · see citing works
Khan, K. N., Masuzaki, H., Fujishita, A., Kitajima, M., Sekine, I., & Ishimaru, T. (2003) · Fertility and Sterility · doi:10.1016/s0015-0282(02)04535-1 · Cited by 78 · see citing works
Proteomic 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
Ming, J., Zhang, Q., Qiu, X., & Wang, E. (2009) · European Journal of Cancer · doi:10.1016/j.ejca.2008.12.006 · Cited by 71 · see citing works
Schulz, M. M. P., Reisen, F., Zgraggen, S., Fischer, S., Yuen, D., Kang, G. J., Chen, L., Schneider, G., & Detmar, M. J. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1206036109 · Cited by 69 · see citing works
Mechsner, S., Weichbrodt, M., Riedlinger, W. F. J., Bartley, J., Kaufmann, A. M., Schneider, A., & Kohler, C. (2008) · Human Reproduction · doi:10.1093/humrep/den259 · Cited by 69 · see citing works
Lymphatic Vessel Dynamics in the Uterine Wall
Red‐Horse, K. (2007) · Placenta · doi:10.1016/j.placenta.2007.11.011 · Cited by 68 · see citing works
Ikeda, Y., Yonemitsu, Y., Onimaru, M., Nakano, T., Miyazaki, M., Kohno, R.-I., Nakagawa, K., Ueno, A., Sueishi, K., & Ishibashi, T. (2006) · Experimental Eye Research · doi:10.1016/j.exer.2006.05.007 · Cited by 65 · see citing works
Lymphangiogensis of normal endometrium and endometrial adenocarcinoma
Donoghue, J. F., Lederman, F. L., Susil, B. J., & Rogers, P. A. W. (2007) · Human Reproduction · doi:10.1093/humrep/dem037 · Cited by 65 · see citing works
Kim, J. G., Suh, C. S., Kim, S. H., Choi, Y. M., Moon, S. Y., & Lee, J. Y. (2000) · Fertility and Sterility · doi:10.1016/s0015-0282(00)00493-3 · Cited by 65 · see citing works
Endometrial receptivity for implantation: Another look at the issue of peri-implantation oestrogen
Ghosh, D., & Sengupta, J. (1995) · Human Reproduction · doi:10.1093/humrep/10.1.1 · Cited by 63 · see citing works
Mouse Model of Surgically-induced Endometriosis by Auto-transplantation of Uterine Tissue
Pelch, K. E., Sharpe-Timms, K. L., & Nagel, S. C. (2012) · Journal of Visualized Experiments · doi:10.3791/3396 · Cited by 62 · see citing works
Sundqvist, J., Andersson, K. L., Scarselli, G. F., Gemzell‐Danielsson, K., & Lalitkumar, P. G. (2012) · Human Reproduction · doi:10.1093/humrep/des220 · Cited by 60 · see citing works
Angiopoietin-1, angiopoietin-2 and Tie-2 expression in eutopic endometrium in advanced endometriosis
Hur, S. E. (2006) · Molecular Human Reproduction · doi:10.1093/molehr/gal049 · Cited by 58 · see citing works
From Anti-Angiogenesis to Anti-Lymphangiogenesis: Emerging Trends in Cancer Therapy
Stacker, S. A., & Achen, M. G. (2008) · Lymphatic Research and Biology · doi:10.1089/lrb.2008.1015 · Cited by 57 · see citing works
Sahni, D., Robson, A., Orchard, G. E., Szydlo, R., Evans, A. V., & Russell‐Jones, R. (2005) · Journal of Clinical Pathology · doi:10.1136/jcp.2004.020123 · Cited by 53 · see citing works
Apoptosis pattern in human endometrium in women with pelvic endometriosis
Szymanowski, K. (2006) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2006.04.008 · Cited by 52 · see citing works
Rectal Surgery for Endometriosis—Should We Be Aggressive?
Varol, N., Maher, P. J., Healey, M., Woods, R., Wood, C. E., Hill, D., Lolatgis, N., & Tsaltas, J. (2003) · The Journal of the American Association of Gynecologic Laparoscopists · doi:10.1016/s1074-3804(05)60296-4 · Cited by 52 · see citing works
Localization of T Cells, Interferon-Gamma and HLA-DR in Eutopic and Ectopic Human Endometrium
Chiang, C. M., & Hill, J. A. (2010) · Gynecologic and Obstetric Investigation · doi:10.1159/000291866 · Cited by 51 · see citing works
Immunohistochemical characterization of leucocyte subpopulations in endometriotic lesions
Oosterlynck, D. J., Cornillie, F. J., Waer, M., & Koninckx, P. R. (1993) · Archives of Gynecology and Obstetrics · doi:10.1007/bf02766646 · Cited by 50 · see citing works
Bruse, C., Bergqvist, A., Carlström, K., Fianu-Jonasson, A., Lecander, I., & Åstedt, B. (1998) · Fertility and Sterility · doi:10.1016/s0015-0282(98)00285-4 · Cited by 50 · see citing works
Effects of simvastatin in prevention of pain recurrences after surgery for endometriosis
Tamannaei, Z. (2013) · Medical Science Monitor · doi:10.12659/msm.883967 · Cited by 50 · see citing works
Endometriosis of the Bowel with Lymph Node Involvement
Insabato, L., & Pettinato, G. (1996) · Pathology - Research and Practice · doi:10.1016/s0344-0338(96)80079-3 · Cited by 46 · see citing works
Milingos, D. S., Philippou, Α., Armakolas, A., Papageorgiou, E. G., Sourla, A., Protopapas, A., Liapi, A., Antsaklis, A. J., Mastrominas, M., & Koutsilieris, M. (2010) · Molecular Medicine · doi:10.2119/molmed.2010.00043 · Cited by 45 · see citing works
Lymphangiogenesis in deep infiltrating endometriosis
Keichel, S., Barcena de Arellano, M. L., Reichelt, U., Riedlinger, W. F. J., Schneider, A., Kohler, C., & Mechsner, S. (2011) · Human Reproduction · doi:10.1093/humrep/der230 · Cited by 44 · see citing works
L1 cell adhesion molecule (L1CAM) as a pathogenetic factor in endometriosis
Finas, D., Huszar, M., Agic, A., Dogan, S., Kiefel, H., Riedle, S., Gast, D., Marcovich, R., NOACK, F., Altevogt, P., et al. (2008) · Human Reproduction · doi:10.1093/humrep/den044 · Cited by 42 · see citing works
Mechsner, S., Weichbrodt, M., Riedlinger, W. F. J., Kaufmann, A. M., Schneider, A., & Köhler, C. (2010) · Fertility and Sterility · doi:10.1016/j.fertnstert.2009.03.097 · Cited by 41 · see citing works
Hapangama, D. K., Turner, M. A., Drury, J. A., Heathcote, L., Afshar, Y., Mavrogianis, P. A., & Fazleabas, A. T. (2010) · Human Reproduction · doi:10.1093/humrep/deq248 · Cited by 41 · see citing works
Mihalich, A., Reina, M., Mangioni, S., Ponti, E., Alberti, L., Viganò, P., Vignali, M., & Blasio, A. M. D. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-021434 · Cited by 41 · see citing works
Peritoneal fluid environment in endometriosis
Bedaiwy, M. A., & Falcone, T. (2003) · Cited by 41 · see citing works
Liu, Y.-H., Lin, C.-Y., Lin, W., Tang, S.-W., Lai, M., & Lin, J. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.9.6584 · Cited by 38 · see citing works
Loverro, G., Maiorano, E., Napoli, A., Selvaggi, L. E., Marra, E., & Perlino, E. (2001) · International Journal of Molecular Medicine · doi:10.3892/ijmm.7.4.423 · Cited by 36 · see citing works
Sbracia, M., Scarpellini, F., Zupi, E., Manna, C., Marconi, D., Romaninï, C., Alò, P., Tondo, U. D., & Grasso, J. (1997) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.1997.tb00238.x · Cited by 36 · see citing works
Elevated levels of fibroblast growth factor-2 in serum from women with endometriosis
Бурлев, В. А., Larsson, A. O., & Olovsson, M. (2006) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2005.08.064 · Cited by 36 · see citing works
Superficial lymphatics in the functional zone of normal human endometrium
Blackwell, P. M., & Fraser, I. S. (1981) · Microvascular Research · doi:10.1016/0026-2862(81)90027-3 · Cited by 33 · see citing works
Lymphatic spread of endometriosis to pelvic sentinel lymph nodes: a prospective clinical study
Tempfer, C. M., Wenzl, R. J., Horvat, R., Grimm, C., Polterauer, S., Buerkle, B., Reinthaller, A., & Huber, J. C. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2011.06.070 · Cited by 32 · see citing works
Hey-Cunningham, A. J., Fazleabas, A. T., Braundmeier, A. G., Markham, R., Fraser, I. S., & Berbic, M. (2011) · Reproductive Sciences · doi:10.1177/1933719110397210 · Cited by 30 · see citing works
Self-citationCould statins constitute a novel treatment for endometriosis? Systematic review of the literature
Gibran, L., Maranhão, R. C., Abrão, M. S., Baracat, E. C., & Podgaec, S. (2014) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2014.05.028 · Cited by 29 · see citing works
Insulin‐Like Growth Factor–1 Isoform mRNA Expression in Women with Endometriosis
Milingos, D. S., Katopodis, H., Milingos, S., Πρωτόπαπας, Α., Creatsas, G. K., Michalas, S., Antsaklis, A. J., & Koutsilieris, M. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1365.042 · Cited by 27 · see citing works
Berbic, M., Ng, C. H. M., Black, K. I., Markham, R., Russell, P., Basten, A., Fraser, I. S., & Hey‐Cunningham, A. J. (2013) · Reproductive Sciences · doi:10.1177/1933719113485298 · Cited by 25 · see citing works
Ellis, H. (2011) · Anaesthesia & intensive care medicine · doi:10.1016/j.mpaic.2010.11.005 · Cited by 25 · see citing works
Wnt1 Is Anti-Lymphangiogenic in a Melanoma Mouse Model
Niederleithner, H., Heinz, M., Tauber, S., Bilban, M., Pehamberger, H., Sonderegger, S., Knöfler, M., Bracher, A., Berger, W., Loewe, R. P., et al. (2012) · Journal of Investigative Dermatology · doi:10.1038/jid.2012.138 · Cited by 23 · see citing works
Endometriosis in para-aortic lymph nodes during pregnancy: case report and review of literature
Beavis, A., Matsuo, K., Grubbs, B. H., Srivastava, S., Truong, C., Moffitt, M. N., Maliglig, A. M., & Lin, Y. G. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2011.01.157 · 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
High Lymph Vessel Density and Expression of Lymphatic Growth Factors in Peritoneal Endometriosis
Reichelt, U., Keichel, S., Barcena, M. L., Chiàntera, V., Schneider, A., & Mechsner, S. (2012) · Reproductive Sciences · doi:10.1177/1933719112438440 · Cited by 22 · see citing works
Chang, S., & Ho, Y. (1997) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.3109/00016349709050064 · Cited by 20 · see citing works
Malignant transformation of abdominal wall endometriosis with lymph node metastasis
Fargas Fàbregas, F., Cusidó Guimferrer, M., Tresserra Casas, F., Baulies Caballero, S., & Fábregas Xauradó, R. (2014) · Gynecologic Oncology Case Reports · doi:10.1016/j.gynor.2013.12.003 · Cited by 19 · see citing works
Methods of detection of lymphatics and their changes with oestrous cycle.
Uchino, S., ICHIKAWA, S., Okubo, M., Nakamura, Y., & Iimura, A. (1987) · PubMed · Cited by 19 · see citing works
Barrier, B. F., Dick, E. J., Butler, S. D., & Hubbard, G. B. (2006) · Human Reproduction · doi:10.1093/humrep/del352 · Cited by 18 · see citing works
Regional lymphatic spread in women with pelvic endometriosis
Gong, Y., & Tempfer, C. M. (2011) · Medical Hypotheses · doi:10.1016/j.mehy.2010.12.018 · Cited by 17 · see citing works
Expression of heparanase and angiopoietin-2 in patients with endometriosis
Jingting, C., Yang-de, Z., Zhang, Y., Li, M., Yu, R., Yu, Z., Guo-qing, P., & Li-xiu, P. (2006) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2006.09.018 · Cited by 16 · see citing works
A 42-Year-Old Woman With a 7-Month History of Abdominal Pain
Sheikh, H. A., Krishnamurti, U., Bhat, Y. M., & Rajendiran, S. (2005) · Archives of Pathology & Laboratory Medicine · doi:10.5858/2005-129-e218-aywwam · Cited by 16 · see citing works
Uterine Lymphatic and Blood Micro-Vessels in Women with Endometriosis through the Menstrual Cycle
Hey-Cunningham, A. J., Ng, F. W., Busard, M. P. H., Berbic, M., Manconi, F., Young, L., Zevallos, H. B.-V., Russell, P., Markham, R., & Fraser, I. S. (2010) · Journal of Endometriosis · doi:10.1177/228402651000200404 · Cited by 16 · see citing works
Self-citationIntraoperative lymphatic mapping techniques for endometrial cancer
Mais, V., Cirronis, M. G., Piras, B., Silvetti, E., Cossu, E., & Melis, G. B. (2010) · Expert Review of Anticancer Therapy · doi:10.1586/era.10.181 · Cited by 14 · see citing works
Trans-Lymphatic Metastasis in Peritoneal Dissemination
Yonemura, Y. (2013) · Journal of Gastrointestinal & Digestive System · doi:10.4172/2161-069x.s12-007 · Cited by 13 · see citing works
TNF system in eutopic endometrium from women with endometriosis
Boric, M. A., Torres, M. J., Pinto, C., Pino, M., Hidalgo, P., Gabler, F., Fuentes, A., & Johnson, M. C. (2013) · Open Journal of Obstetrics and Gynecology · doi:10.4236/ojog.2013.32051 · Cited by 11 · see citing works
The endometrial lymphatic vasculature: Function and dysfunction
Girling, J. E., & Rogers, P. A. W. (2012) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-012-9224-6 · Cited by 11 · see citing works
Ganewatta, S. P., Berbic, M., Luscombe, G. M., Markham, R., & Fraser, I. S. (2010) · Journal of Endometriosis and Pelvic Pain Disorders · doi:10.1177/228402651000200403 · Cited by 11 · see citing works
Peritoneal Fluid Environment in Endometriosis
Berger, N. A., & Rock, J. A. (1985) · Seminars in Reproductive Medicine · doi:10.1055/s-2007-1022632 · Cited by 9 · see citing works
ENDOMETRIOSIS OF THE PELVIC LYMPH NODES
Aoki, M. (1967) · Acta Pathologica Japonica · doi:10.1111/j.1440-1827.1967.tb03169.x · Cited by 9 · see citing works
Immunolocalization of angiopoietin 1 in human peritoneal endometriotic lesions
Gescher, D. M., Berndorff, U., Meyhöfer-Malik, A., Moubayed, P., & Malik, E. (2004) · Fertility and Sterility · doi:10.1016/j.fertnstert.2003.09.032 · Cited by 8 · see citing works
Histological characteristics of healthy animal peritoneum
Stankovic, J. T., Nešić, D., Lausevic, Z., Obradović, M., Brajušković, G. N., & Biljana, S. (2006) · Acta veterinaria · doi:10.2298/avb0606405t · Cited by 7 · see citing works
Lymphatic Vessels in Peritoneal Endometriotic Lesions
Hey-Cunningham, A. J., Berbic, M., Ng, C. H. M., Markham, R., & Fraser, I. S. (2011) · Journal of Endometriosis · doi:10.5301/je.2011.8522 · Cited by 7 · see citing works
Compilation of Paintings on the Normal and Pathologic Anatomy of the Reproductive System
Netter, F. H., Oppenheimer, E., & Velardo, J. T. (1956) · Anesthesiology · doi:10.1097/00000542-195601000-00025 · Cited by 6 · see citing works
Endometriosis and regional lymph node involvement in a rat model
Gong, Y., Hong, L., Zheng, C., Tong, X., & Tempfer, C. M. (2011) · Wiener klinische Wochenschrift · doi:10.1007/s00508-011-0003-2 · Cited by 3 · see citing works
Does lymphatic growth rely on Immune cell function?
Ivanov, S., & Martel, C. (2013) · OA Immunology · doi:10.13172/2052-9295-1-1-1113 · Cited by 2 · see citing works
Ellis, H. (2008) · Anaesthesia & intensive care medicine · doi:10.1016/j.mpaic.2008.01.010 · Cited by 2 · see citing works
Flagged first, then by citations
1 of the 153 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Zondervan, K. T., Becker, C. M., & Missmer, S. A. (2020) · New England Journal of Medicine · doi:10.1056/nejmra1810764 · Cited by 2,249 · see citing works
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 · see citing works
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 527 · see citing works
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 · see citing works
“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).”
BackgroundThe 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 · see citing works
“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].”
BackgroundExtrapelvic 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 · see citing works
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 · see citing works
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 175 · see citing works
“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].”
BackgroundHung, 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 171 · see citing works
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 · see citing works
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 121 · see citing works
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 108 · see citing works
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 99 · see citing works
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 · see citing works
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 70 · see citing works
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 66 · see citing works
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 · see citing works
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 · see citing works
“The lymphatic dissemination theory has been proposed to explain the observations of endometrial tissue moving through the vasculature and lymph nodes [30].”
BackgroundAltered 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 · see citing works
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 · see citing works
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 · see citing works
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 44 · see citing works
Borghese, B., Santulli, P., Marcellin, L., & Chapron, C. (2018) · Gynécologie Obstétrique Fertilité & Sénologie · doi:10.1016/j.gofs.2018.02.017 · Cited by 42 · see citing works
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 · see citing works
Tang, H., Lin, T., Wu, M., & Tsai, S. (2024) · Reproductive Medicine and Biology · doi:10.1002/rmb2.12588 · Cited by 42 · see citing works
Endometriosis and inflammatory immune responses: Indian experience
Gajbhiye, R. (2022) · American Journal of Reproductive Immunology · doi:10.1111/aji.13590 · Cited by 36 · see citing works
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 32 · see citing works
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 · see citing works
Endometriosis origin from primordial germ cells
Makiyan, Z. (2017) · Organogenesis · doi:10.1080/15476278.2017.1323162 · Cited by 31 · see citing works
“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…”
BackgroundLymphatic 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 30 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Koyama, R., Aiyama, T., Yokoyama, R., & Nakano, S. (2021) · American Journal of Case Reports · doi:10.12659/ajcr.930141 · Cited by 19 · see citing works
“Emerging evidence suggests that the lymphatic system is deeply involved in the pathogenesis and progression of endometriosis [11].”
BackgroundHarmsen, 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 · see citing works
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 · see citing works
“Similarly, these endometrial cells can also circulate to ectopic sites via vascular dissemination [6].”
BackgroundDigestive system deep infiltrating endometriosis: What do we know
Yin, W., Li, X., Liu, P., Li, Y.-J., Liu, J., Yu, S., & Tai, S. (2023) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.17921 · Cited by 16 · see citing works
“60 Other lymphangiogenic factors were also found in DIE lesions, such as VEGF-A, VEGFR-2.”
BackgroundResultInfluentialEmerging 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 · see citing works
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 · see citing works
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 · see citing works
“Additionally, EMs causes lymph node immune response deficiency and insufficient clearance of endometrial cells, resulting in EMs metastasis [16].”
BackgroundMicrobiota 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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Otsuka, I. (2023) · Cancers · doi:10.3390/cancers15184614 · Cited by 9 · see citing works
“Endometriosis is believed to disseminate via the lymphatic system [141].”
BackgroundActual 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 · see citing works
Russell, P., & Anderson, L. A. (2015) · Pathology · doi:10.1016/j.pathol.2015.11.024 · Cited by 9 · see citing works
Yang, H. (2024) · Frontiers in Medicine · doi:10.3389/fmed.2024.1434582 · Cited by 8 · see citing works
Arsalan, H. M., Mumtaz, H., & Laganà, A. S. (2025) · Advances in clinical chemistry · doi:10.1016/bs.acc.2025.01.004 · Cited by 8 · see citing works
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 · see citing works
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 · see citing works
“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].”
InfluentialRetractedEndometriosis 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 · see citing works
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 · see citing works
“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].”
BackgroundYu, F., Zhu, Y., Shang, X., Yuan, H., & Hu, F. (2022) · Current Medicinal Chemistry · doi:10.2174/0929867329666220620164429 · Cited by 8 · see citing works
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 7 · see citing works
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 7 · see citing works
“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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 6 · see citing works
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 7 · see citing works
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 · see citing works
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 · see citing works
Jin, Z., Zhang, Y., Li, J., Lv, S., Zhang, L., & Feng, Y. (2021) · Regenerative Medicine · doi:10.2217/rme-2021-0039 · Cited by 4 · see citing works
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 4 · see citing works
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 · see citing works
Yang, H. (2024) · Polish Journal of Microbiology · doi:10.33073/pjm-2024-041 · Cited by 3 · see citing works
“…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 · see citing works
“Endometriotic cells may also be distributed to ectopic sites via lymphovascular metastasis [5].”
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 · see citing works
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 · see citing works
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 · see citing works
“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].”
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 · see citing works
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 · see citing works
Endometriosis and the Hallmarks of Cancer
Ellis, K. B., & Wood, R. (2025) · Reproductive Sciences · doi:10.1007/s43032-025-02024-0 · Cited by 3 · see citing works
Hays, B. M., & Hudson, T. (2020) · Elsevier eBooks · doi:10.1016/b978-0-323-43044-9.00166-7 · Cited by 2 · see citing works
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 · see citing works
“…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 · see citing works
(2022) · International Journal of Biology Pharmacy and Allied Sciences · doi:10.31032/ijbpas/2022/11.6.6172 · Cited by 1 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
“12 The ovary is the most common site of ectopic endo-metriotic implantation.”
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 · see citing works
“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 · see citing works
Simpson, P., Tyler, X., & Morris, E. (2016) · Gynecological Surgery · doi:10.1007/s10397-016-0984-y · Cited by 1 · see citing works
“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.”
BackgroundEndometriosis 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 · see citing works
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 · see citing works
“…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).”
BackgroundHamdy, 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 · see citing works
Melkozerova, O. A. (2018) · Journal of Gynecology and Obstetrics · doi:10.11648/j.jgo.20180604.15 · Cited by 1 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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].”
BackgroundInfluentialLi, 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
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
- 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 › Surgery › 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