Estrogen and progestogen receptor positive endometriotic lesions and disseminated cells in pelvic sentinel lymph nodes of patients with deep infiltrating rectovaginal endometriosis: a pilot study
Abstract
BACKGROUND: Deep infiltrating endometriosis (DIE) shows similarities to malignant diseases. A recent study involving DIE patients found endometriosis in mesorectal lymph nodes (LNs) after segmental bowel resection. However, it is unclear whether this observation is a local phenomenon or a sign of systemic disease. Therefore, we conducted a prospective study to investigate the occurrence of endometriosis in pelvic sentinel lymph nodes (SLNs) in patients with DIE. METHODS: Fourteen patients underwent primary surgery for symptomatic DIE. Combined vaginal laparoscopic-assisted resection of the rectovaginal septum was performed. Dye was injected into the visible/palpable nodule. SLNs were removed from the iliac region. In order to identify endometriotic cells, immunohistochemical analysis of estrogen and progestogen receptors, CD10 and cytokeratin was performed. RESULTS: In 12 out of 14 patients with DIE, SLNs were detected. The localization of the SLN followed the typical LN spread of the upper vagina. In three patients, we could detect typical endometriotic lesions in the LNs. Ten out of 12 (83.3%) SLNs showed disseminated estrogen and/or progestogen positive cells. CONCLUSIONS: By using immunohistochemistry, we could demonstrate endometriotic lesions and endometriotic-like cells in pelvic SLNs of patients with DIE suggesting the potential for lymphatic spread of the disease.
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 [17]
Cites
Giudice, L. C., & Kao, L. C. (2004) · The Lancet · doi:10.1016/s0140-6736(04)17403-5 · Cited by 3,166 · see citing works
Revised American Society for Reproductive Medicine classification of endometriosis: 1996
American Society for Reproductive Medicine (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)81391-x · Cited by 3,018 · see citing works
Chapron, C., Fauconnier, A., Vieira, M., Barakat, H., Dousset, B. E., Pansini, V., Vacher‐Lavenu, M., & Dubuisson, J. B. (2003) · Human Reproduction · doi:10.1093/humrep/deg009 · Cited by 584 · see citing works
Relation between pain symptoms and the anatomic location of deep infiltrating endometriosis
Fauconnier, A., Chapron, C., Dubuisson, J.-B., Vieira, M., Dousset, B., & Bréart, G. (2002) · Fertility and Sterility · doi:10.1016/s0015-0282(02)03331-9 · Cited by 498 · see citing works
The effect of endometriosis and its radical laparoscopic excision on quality of life indicators
Garry, R., Clayton, R., & Hawe, J. (2000) · BJOG: An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.2000.tb11578.x · Cited by 299 · see citing works
Multicenter Validation Study of the Sentinel Lymph Node Concept in Cervical Cancer: AGO Study Group
Altgassen, C., Hertel, H., Brandstädt, A., et al. (2008) · Journal of Clinical Oncology · doi:10.1200/jco.2007.13.8933 · Cited by 295 · see citing works
Quality of life after laparoscopic colorectal resection for endometriosis
Dubernard, G., Piketty, M., Rouzier, R., Houry, S., Bazot, M., & Darai, E. (2006) · Human Reproduction · doi:10.1093/humrep/dei491 · Cited by 272 · see citing works
INTESTINAL ENDOMETRIOSIS: A Report of 29 Cases and a Survey of the Literature
Macafee, C. H. G., & Greer, H. L. H. (1960) · BJOG: An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1960.tb09211.x · Cited by 266 · see citing works
ENZIAN-Score, eine Klassifikation der tief infiltrierenden Endometriose
Tuttlies, F., Keckstein, J., Ulrich, U., Possover, M., Schweppe, K., Wustlich, M., Buchweitz, O., Greb, R., Kandolf, O., Mangold, R., et al. (2005) · Zentralblatt für Gynäkologie · doi:10.1055/s-2005-836904 · Cited by 233 · see citing works
Weed, J. C., & Ray, J. E. (1987) · PubMed · Cited by 228 · see citing works
Aggressive surgical management for advanced colorectal endometriosis
Bailey, R. H., Ott, M. T., & Hartendorp, P. (1994) · Diseases of the Colon & Rectum · doi:10.1007/bf02050136 · Cited by 224 · see citing works
Köhler, C., Klemm, P., Schau, A., et al. (2004) · Gynecologic Oncology · doi:10.1016/j.ygyno.2004.07.025 · Cited by 199 · see citing works
Sumathi, V. P., & McCluggage, W. G. (2002) · Journal of Clinical Pathology · doi:10.1136/jcp.55.5.391 · Cited by 197 · see citing works
Surgical treatment of symptomatic colorectal endometriosis
Coronado, C., Franklin, R. R., Lotze, E. C., Bailey, H. R., & Valdés, C. T. (1990) · Fertility and Sterility · doi:10.1016/s0015-0282(16)53332-9 · Cited by 189 · see citing works
LAPAROSCOPICALLY ASSISTED VAGINAL RESECTION OF RECTOVAGINAL ENDOMETRIOSIS
Possover, M., Diebolder, H., Plaul, K., & Schneider, A. (2000) · Obstetrics and Gynecology · doi:10.1016/s0029-7844(00)00839-5 · Cited by 168 · see citing works
Self-citationFord, 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
Laparoscopic management of colorectal endometriosis
Jerby, B. L., Kessler, H. P., Falcone, T., & Milsom, J. W. (1999) · Surgical Endoscopy · doi:10.1007/s004649901187 · Cited by 157 · see citing works
Hyperestrogenism: A Relevant Risk Factor for the Development of Cancer from Endometriosis
Zanetta, G. M., Webb, M. J., Li, H., & Keeney, G. L. (2000) · Gynecologic Oncology · doi:10.1006/gyno.2000.5905 · Cited by 156 · see citing works
Topographic distribution of sentinel lymph nodes in patients with cervical cancer
Marnitz, S., Köhler, C., Bongardt, S., et al. (2006) · Gynecologic Oncology · doi:10.1016/j.ygyno.2006.01.061 · Cited by 150 · see citing works
Malignancy arising in extragonadal endometriosis.A case report and summary of the world literature
Brooks, J. J. S., & Wheeler, J. E. (1977) · Cancer · doi:10.1002/1097-0142(197712)40:6 · Cited by 147 · see citing works
Lymphatic system of the female genitalia. The morphologic basis of oncologic diagnosis and therapy.
Plentl, A. A., & Friedman, E. A. (1971) · PubMed · Cited by 129 · see citing works
Book Review: Lymphatic System of the Female Genitalia
Hudson, C. N. (1972) · Proceedings of the Royal Society of Medicine · doi:10.1177/003591577206500954 · Cited by 128 · see citing works
Chapron, C., Jacob, S., Dubuisson, J., Vieira, M., Liaras, E., & Fauconnier, A. (2001) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1034/j.1600-0412.2001.080004349.x · Cited by 122 · see citing works
Deeply infiltrating endometriosis affecting the rectum and lymph nodes
Abrão, M. S., Podgaec, S., Dias, J., Averbach, M., Garry, R., da Silva, L. F. F., & Carvalho, F. M. (2006) · Fertility and Sterility · doi:10.1016/j.fertnstert.2006.02.102 · Cited by 107 · see citing works
Fujishita, A., Nakane, P. K., Koji, T., Masuzaki, H., Chavez, R. O., Yamabe, T., & Ishimaru, T. (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)81397-0 · Cited by 99 · see citing works
Evidence that Endometriosis Behaves in a Malignant Manner
Thomas, E. J., & Campbell, I. (2000) · Gynecologic and Obstetric Investigation · doi:10.1159/000052872 · Cited by 87 · see citing works
Lymph node involvement and lymphovascular invasion in deep infiltrating rectosigmoid endometriosis
Noël, J., Chapron, C., Fayt, I., & Anaf, V. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.05.011 · Cited by 81 · see citing works
Cytokeratin-Positive Malignant Tumors With Reticulum Cell Morphology
Chan, A. C. L., Serrano‐Olmo, J., Erlandson, R. A., & Rosaí, J. (2000) · The American Journal of Surgical Pathology · doi:10.1097/00000478-200001000-00013 · Cited by 65 · see citing works
Parametrial and rectovaginal adenocarcinoma arising from endometriosis
Ulrich, U. A., Rhiem, K., KAMINSKI, M., Wardelmann, E., Trog, D., Valter, M. M., & RICHTER, O. N. (2005) · International Journal of Gynecological Cancer · doi:10.1111/j.1525-1438.2005.00184.x · Cited by 54 · 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
Benign CD10-Positive T Cells in Reactive Lymphoid Proliferations and B-Cell Lymphomas
Cook, J. R., Craig, F. E., & Swerdlow, S. H. (2003) · Modern Pathology · doi:10.1097/01.mp.0000084630.64243.d1 · Cited by 47 · see citing works
The use of sentinel lymph nodes in gynaecological malignancies
Torné, A., & Puig-Tintoré, L. M. (2004) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/00001703-200402000-00011 · Cited by 43 · see citing works
Zanetti‐Dällenbach, R., Bartley, J., Müller, C., Schneider, A., & Köhler, C. (2007) · Surgical Endoscopy · doi:10.1007/s00464-007-9560-x · Cited by 42 · see citing works
Self-citationDas Lymphsystem des weiblichen Genitale
Reiffenstuhl, G. (1957) · Urban & Schwarzenberg eBooks · Cited by 39 · see citing works
A Rare Case of Rectovaginal Endometriosis with Lymph Node Involvement
Thomakos, N., Rodolakis, A., Vlachos, G. D., Papaspirou, I., Markaki, S. P., & Antsaklis, A. J. (2006) · Gynecologic and Obstetric Investigation · doi:10.1159/000091998 · Cited by 25 · see citing works
Onda, T., Ban, S., & Shimizu, M. (2002) · Journal of Clinical Pathology · doi:10.1136/jcp.56.1.79-a · Cited by 24 · see citing works
Primary adenocarcinoma of the rectovaginal septum: a case report and literature review
Berger, A., Rouzier, R., Carnot, F., Braunberger, E., Cugnenc, P., & Danel, C. J. (2001) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/s0301-2115(00)00377-8 · Cited by 22 · 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
Ulrich, U. A., Richter, O., Wardelmann, E., Valter, M., Schmutzler, R., Sillem, M., Possover, M., & Mallmann, P. (2003) · Zentralblatt für Gynäkologie · doi:10.1055/s-2003-42277 · Cited by 16 · see citing works
Tzankov, A., Krugmann, J., & Mikuz, G. (2002) · Journal of Clinical Pathology · doi:10.1136/jcp.56.1.79 · Cited by 2 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Zondervan, K. T., Becker, C. M., Koga, K., Missmer, S. A., Taylor, R. N., & Viganò, P. (2018) · Nature Reviews Disease Primers · doi:10.1038/s41572-018-0008-5 · Cited by 1,257 · 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
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
Estrogen metabolism and action in endometriosis
Rižner, T. L. (2009) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2009.03.022 · Cited by 153 · see citing works
The Role of the Lymphatic System in Endometriosis: A Comprehensive Review of the Literature1
Jerman, L. F., & Hey-Cunningham, A. J. (2015) · Biology of Reproduction · doi:10.1095/biolreprod.114.124313 · Cited by 122 · 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
Self-citationMechsner, 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
Self-citationHey-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
Liu, G., Wang, Y., Chen, Y., & Ren, F. (2021) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2021.08.006 · Cited by 25 · 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
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
Riedlinger, W. F. J., Weichbrodt, M., Gericke, J., Gericke, C., Schneider, A., Köhler, C., & Mechsner, S. (2010) · Journal of Endometriosis · doi:10.1177/228402651000200106 · Cited by 5 · see citing works
Self-citation
- Authors
- Mechsner, S., Weichbrodt, M., Riedlinger, W. F. J., Bartley, J., Kaufmann, A. M., Schneider, A., & Kohler, C.
- Affiliations
- Stiftung Charité (DE)
- Venue
- Human Reproduction
- Publisher
- Oxford University Press (OUP)
- Published
- 2008-07-08
- Volume
- 23
- Issue
- 10
- Pages
- 2202-2209
- ISSN
- 0268-1161 (ISSN-L)
- 1460-2350
- OpenAlex
- W2134906914
- Cited by
- 69
- References
- 40
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 1 · 2023: 5 · 2022: 7 · 2021: 6 · 2020: 8 · 2019: 2 · 2018: 3 · 2017: 1 · 2016: 5 · 2015: 4 · 2014: 2 · 2013: 4 · 2012: 3
- FWCI
- 5.79
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Human Reproduction (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Health Sciences › Medicine › Obstetrics and Gynecology › Endometrial and Cervical Cancer Treatments
- Health Sciences › Medicine › Obstetrics and Gynecology › Gynecological conditions and treatments
- Keywords
- deep infiltrating endometriosis, rectovaginal endometriosis, sentinel lymph node, lymphatic spread, estrogen receptor, progestogen receptor, endometriotic cells, CD10, cytokeratin, lymph node metastasis
- MeSH terms
- Adult, Endometriosis, Female, Humans, Immunohistochemistry, Lymph Nodes, Middle Aged, Pelvis, Pilot Projects, Prospective Studies, Receptors, Estrogen, Receptors, Steroid, Rectal Diseases, Gynecologic Surgical Procedures, Vaginal Diseases, Ki-67 Antigen, Sentinel Lymph Node Biopsy
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
