Transcoelomic and Lympho-Hematogenous Dissemination of Endometrioid Heterotopias – the Mechanism of Extragenital Endometriosis Formation

In: Journal of Anatomy and Histopathology · 2021 · vol. 10(1) , pp. 85–91 · doi:10.18499/2225-7357-2021-10-1-85-91 · W3160390249
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This article demonstrates how endometrioid cells spread via lymphatic, hematogenous, and transcoelomic routes, supporting the theory of utero-peritoneal reflux as a primary mechanism for extragenital endometriosis formation.

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The paper discusses the proposed mechanisms for dissemination of endometrioid heterotopias that lead to extragenital endometriosis, emphasizing transcoelomic spread and lympho-hematogenous dissemination in the body. It argues that endometriotic lesions have more developed lymphatic networks than normal endometrium due to active lymphangiogenesis, and that invasive growth allows dissemination along lymphatic outflow pathways from typical pelvic locations to affect inguinal and pelvic lymph nodes. The authors explicitly note that adenomyosis-associated lymphatic dissemination is reported in one-quarter of patients and claim that this may require changes to surgical protocols involving regional lymph node excision, while also pointing to pulmonary and hepatic endometriosis as support for hematogenous spread; however, the text is largely explanatory and does not describe a specific original study design. This paper is centrally about endometriosis — it focuses on mechanisms of extragenital endometriosis formation via transcoelomic and lympho-hematogenous dissemination and discusses adenomyosis-associated lymphatic spread as part of the proposed model.

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Abstract

Endometriosis nowadays still a disease with an undisclosed pathogenesis. This article demonstrates and explains the possibility of different variants of dissemination of endometrioid cells in the body with the formation of foci of extragenital endometriosis in organs and tissues remote from the pelvis, complementing and confirming the theory of utero-peritoneal reflux in the development of endometriosis as the most reasonable. Endometrioid heterotopias have a more developed lymphatic network compared to the normal endometrium due to active lymphangiogenesis, and, having a tendency to invasive growth, endometrioid heterotopia is a source of endometrioid cells spreading along the direction of lymph outflow from the most typical locations (pelvic organs) with damage to the inguinal and pelvic lymph nodes. Lymphatic dissemination in adenomyosis is observed in every fourth patient, which requires revision of the surgery protocol with excision of regional lymph nodes to prevent relapses. The presence of cases of pulmonary endometriosis and endometrioid liver cysts makes hematogenic dissemination of endometriosis from the primary source in the pelvic region obvious. The most frequent localizations of endometrioid heterotopias are located near the corresponding venous plexuses of the small pelvis, the outflow from which occurs mainly through the inferior vena cava, without anatomical obstacles for hematogenic dissemination of endometrioid cells with subsequent lung damage. For liver involment, it is likely that endometriosis in the distal parts of the colon is important, the venous outflow from which is directed to the portal vein system. Endometriosis of the diaphragm – is an example transcoelomic spread with predominant location on the right dome of the diaphragm, as the right subphrenic space communicates with the pelvic cavity through the right lateral channel, which justifies the possibility of such involments of the diaphragme in context of the theory of uteroperitoneal reflux.Thus, the theory of menstrual regurgitation and the theory of hemato-lymphatic dissemination are components of a single pathogenetic model of the distribution of endometrioid cells in the body.
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Трансцеломическая и лимфо-гематогенная диссеминация эдометриоидных гетеротопий – механизм формирования экстрагенитальных форм эндометриоза https://doi.org/10.18499/2225-7357-2021-10-1-85-91 Аннотация Эндометриоз в настоящее время продолжает оставаться заболеванием с нераскрытым патогенезом. Данная статья демонстрирует и обьясняет возможность различных вариантов диссеминации эндометриоидных клеток в организме с формированием очагов экстрагенитального эндометриоза в отдаленных от малого таза органах и тканях, дополняя и подтверждая теорию маточно-перитонеального рефлюкса в развитии эндометриоза как наиболее обоснованную. Эндометриоидные гетеротопии имеют более развитую лимфатическую сеть по сравнению с нормальным эндометрием за счет активного лимфангиогенеза. Обладая склонностью к инвазивному росту, эндометриоидная гетеротопия является источником распространения эндометриоидных клеток по ходу оттока лимфы из наиболее типичных локализаций (органов малого таза) с поражением паховых лимфатических узлов и малого таза. Лимфатическая диссеминация при аденомиозе наблюдается у каждой четвертой пациентки, что требует пересмотра протокола операции с иссечением регионарных лимфатических узлов для предотвращения рецидивов. Наличие случаев легочного эндометриоза и эндометриоидных кист печени делает гематогенную диссеминацию эндометриоза из первоисточника в области малого таза очевидной. Наиболее частые локализации эндометриоидных гетеротопий располагаются возле соответствующих венозных сплетений малого таза, отток от которых происходит преимущественно через нижнюю полую вену, не имея анатомических препятствий для гематогенной диссеминации эндометриоидных клеток с последующим поражением легких. Для поражения печени, вероятно, имеет значение эндометриоидное поражение дистальных отделов толстой кишки, венозный отток от которых направляется в систему воротной вены. Эндометриоз диафрагмы – пример трансцеломического распространения данной патологии с примущественным поражением правого купола диафрагмы, поскольку правое поддиафрагмальное пространство сообщается с полостью малого таза посредством правого бокового канала, что оправдывает возможность подобного поражения в рамках теории маточно-перитонеального рефлюкса. Таким образом, теория менструальной регургитации и теория гемато-лимфатической диссеминации являются составными элементами единой патогенетичексой модели распространения эндометриоидных клеток в организме. Об авторах Р. В. УкраинецРоссия Смоленск Ю. С. Корнева Россия Корнева Юлия Сергеевна ул. Крупской, 28, Смоленск, 214019 Список литературы 1. Аничков Н.М., Печеникова В.А., Костючек Д.Ф. Клинико-морфологические особенности эндометриоидной болезни: аденомиоза, эндометриоза яичников, экстрагенитального эндометриоза. Архив патологии. 2011;73(4):5– 10. [Anichkov NM, Pechenikova VA, Kostiuchek DF. Clinico-Morphological Features of Endometrioid Disease: Adenomyosis, Ovarian Endometriosis, Extragenital Endometriosis. Arhiv patologii. 2011;73(4):5–10] (in Russian). 2. Бессмертная В.С., Галил-Оглы Г.А., Самойлов М.В. Эндометриоз сигмовидной кишки. Архив патологии. 2005;67(3):43 [.Bessmertnaya УS, Galil-Ogly GA, Samoilov MУ. Sygmoid Endometriosis. Arhiv patologii. 2005;67(3):43] (in Russian). 3. Abrao MS, Podgaec S, Dias JA, Averbach M, Garry R, Ferraz Silva LF, et al. Deeply infiltrating endometriosis affecting the rectum and lymph nodes. Fertility and Sterility. 2006 Sep;86(3):543–7. doi: 10.1016/j.fertnstert.2006.02.102 4. Alwadhi S, Kohli S, Chaudhary B, Gehlot K. Thoracic Endometriosis-A Rare Cause of Haemoptysis. J Clin Diagn Res. 2016;10(4): TD01- 2. doi: 10.7860/JCDR/2016/16365.7530 5. Asran M, Rashid A, Szklaruk J. Hepatic Endometriosis Mimicking Metastatic Disease: A Case Report and Review of the Literature. Journal of Radiology Case Reports. 2010 Nov 14;4(11). doi: 10.3941/jrcr.v4i11.589 6. Bourdel N, Fava V, Budianu M-A, Chauvet P, Canis M, Chadeyras J-B. Laparoscopic Resection of Diaphragmatic Endometriosis in 10 Steps. Journal of Minimally Invasive Gynecology. 2019 Nov;26(7):1224–55. doi: 10.1016/j.jmig.2019.04.008 7. Bricou A, Batt RE, Chapron C. Peritoneal fluid flow influences anatomical distribution of endometriotic lesions: Why Sampson seems to be right. European Journal of Obstetrics & Gynecology and Reproductive Biology. 2008 Jun 1;138(2):127–34. doi: 10.1016/j.ejogrb.2008.01.014 8. Fimmanò A, Coppola Bottazzi E, Cirillo C, Tammaro P, Di Carlo R. Inguinal endometriosis. Chir Ital. 2005;57(2):211–14. 9. Gaichies L, Blouet M, Comoz F, Foulon A, Heyndrickx M, Fauvet R. Non-traumatic diaphragmatic rupture with liver herniation due to endometriosis: A rare evolution of the disease requiring multidisciplinary management. Journal of Gynecology Obstetrics and Human Reproduction. 2019 Nov;48(9):785–8. doi: 10.1016/j.jogoh.2019.03.006 10. Gong Y, Tempfer CB. Regional lymphatic spread in women with pelvic endometriosis. Medical Hypotheses. 2011 Apr;76(4):560–3. doi: 10.1016/j.mehy.2010.12.018 11. Ha JK, Choi CW, Kim HW, Kang DH, Park SB, Kim SJ, et al. An Extremely Rare Case of Gastric Subepithelial Tumor: Gastric Endometriosis. Clinical Endoscopy. 2015;48(1):74. doi: 10.5946/ce.2015.48.1.74 12. Hsu M, Terris B, Wu T-T, Zen Y, Eng H-L, Huang W-T, et al. Endometrial cysts within the liver: a rare entity and its differential diagnosis with mucinous cystic neoplasms of the liver. Human Pathology. 2014 Apr;45(4):761–7. doi: 10.1016/j.humpath.2013.11.005 13. Hwang SM, Lee CW, Lee BS, Park JH. Clinical features of thoracic endometriosis: A single center analysis. Obstetrics & Gynecology Science. 2015;58(3):223. doi: 10.5468/ogs.2015.58.3.223 14. Ishibashi N, Tabata T, Koyanagi A, Nonomura R, Sasaki T, Mitomo H, et al. Clinical Assessment of Fourteen Cases of Thoracic Endometriosis. Kyobu Geka. 2019;72(2):87–91. 15. Jerman LF, Hey-Cunningham AJ. The Role of the Lymphatic System in Endometriosis: A Comprehensive Review of the Literature1. Biology of Reproduction. 2015 Mar 1;92(3):64. doi: 10.1095/biolreprod.114.124313 16. Kashyap P, Medeiros F, Levy M, Larson M. Unusual Submucosal Tumor in the Stomach. Gastroenterology. 2011 Jun;140(7):e7–8. doi: 10.1053/j.gastro.2010.03.081 17. Keichel S, Barcena de Arellano M-L, Reichelt U, Riedlinger WFJ, Schneider A, Kohler C, et al. Lymphangiogenesis in deep infiltrating endometriosis. Human Reproduction. 2011 Jul 25;26(10):2713–20. doi: 10.1093/humrep/der230 18. Khan AW, Craig M, Jarmulowicz M, Davidson BR. Liver tumours due to endometriosis and endometrial stromal sarcoma. HPB. 2002 Mar;4(1):43–5. doi: 10.1080/136518202753598735 19. Kumakiri J, Kumakiri Y, Miyamoto H, Kikuchi I, Arakawa A, Kitade M, et al. Gynecologic Evaluation of Catamenial Pneumothorax Associated with Endometriosis. Journal of Minimally Invasive Gynecology. 2010 Sep;17(5):593–9. doi: 10.1016/j.jmig.2010.04.011 20. Li F, Alderman MH, Tal A, Mamillapalli R, Coolidge A, Hufnagel D, et al. Hematogenous Dissemination of Mesenchymal Stem Cells from Endometriosis. STEM CELLS. 2018 Mar 1;36(6):881–90. doi: 10.1002/stem.2804 21. Mascaretti G, Patacchiola F, Di Berardino C, Moscarini M. Isolated inguinal endometriosis. Report of a clinical case. Minerva Ginecol. 2000 Jun;52(6):249–52. 22. Mechsner S, Weichbrodt M, Riedlinger WFJ, Bartley J, Kaufmann AM, Schneider A, et al. 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. Human Reproduction. 2008 Jul 8;23(10):2202–9. doi: 10.1093/humrep/den259 23. Mechsner S, Weichbrodt M, Riedlinger WFJ, Kaufmann AM, Schneider A, Köhler C. Immunohistochemical evaluation of endometriotic lesions and disseminated endometriosis-like cells in incidental lymph nodes of patients with endometriosis. Fertility and Sterility. 2010 Jul;94(2):457–63 doi: 10.1016/j.fertnstert.2009.03.097 24. Nezhat C, Kazerooni T, Berker B, Lashay N, Fernandez S, Marziali M. Laparoscopic management of hepatic endometriosis: Report of two cases and review of the literature. Journal of Minimally Invasive Gynecology. 2005 Jun;12(3):196–200. doi: 10.1016/j.jmig.2005.03.015 25. Noël J-C, Chapron C, Fayt I, Anaf V. Lymph node involvement and lymphovascular invasion in deep infiltrating rectosigmoid endometriosis. Fertility and Sterility. 2008 May;89(5):1069–72. doi: 10.1016/j.fertnstert.2007.05.011 26. Pankratjevaite L, Samiatina-Morkuniene D. A case report of thoracic endometriosis – A rare cause of haemothorax. International Journal of Surgery Case Reports. 2017;33:139–42. doi: 10.1016/j.ijscr.2017.02.052 27. Plodeck V, Sommer U, Baretton GB, Aust DE, Laniado M, Hoffmann R-T, et al. A rare case of pancreatic endometriosis in a postmenopausal woman and review of the literature. Acta Radiologica Open. 2016 Sep;5(9):205846011666938. doi: 10.1177/2058460116669385 28. Prodromidou A, Machairas N, Paspala A, Hasemaki N, Sotiropoulos GC. Diagnosis, surgical treatment and postoperative outcomes of hepatic endometriosis: A systematic review. Annals of Hepatology. 2020 Jan;19(1):17–23. doi: 10.1016/j.aohep.2019.08.006 29. Redwine DB. Diaphragmatic endometriosis: diagnosis, surgical management, and long-term results of treatment. Fertility and Sterility. 2002 Feb;77(2):288–96. doi: 10.1016/s0015-0282(01)02998-3 30. Reichelt U, Keichel S, de Arellano MLB, Chiantera V, Schneider A, Mechsner S. High Lymph Vessel Density and Expression of Lymphatic Growth Factors in Peritoneal Endometriosis. Reproductive Sciences. 2012 Apr 26;19(8):876–82. doi: 10.1177/1933719112438440 31. Roberts LM, Redan J, Reich H. Extraperitoneal endometriosis with catamenial pneumothoraces: a review of the literature. JSLS. 2003;7(4):371–5. 32. Rogers PAW, Donoghue JF, Walter LM, Girling JE. Endometrial Angiogenesis, Vascular Maturation, and Lymphangiogenesis. Reproductive Sciences. 2009 Feb;16(2):147–51. doi: 10.1177/1933719108325509 33. Roman H, Darwish B, Provost D, Baste J-M. Laparoscopic management of diaphragmatic endometriosis by three different approaches. Fertility and Sterility. 2016 Aug;106(2):e1. doi: 10.1016/j.fertnstert.2016.03.051 34. Samani EN, Mamillapalli R, Li F, Mutlu L, Hufnagel D, Krikun G, et al. Micrometastasis of endometriosis to distant organs in a murine model. Oncotarget. 2017 Apr 6;10(23):2282–91. doi: 10.18632/oncotarget.16889 35. Sanada T, Park J, Hagiwara M, Ikeda N, Nagai T, Matsubayashi J, et al. CT and MRI findings of bronchopulmonary endometriosis: a case presentation. Acta Radiologica Open. 2018 Oct;7(10):205846011880116. doi: 10.1177/2058460118801164 36. Schuld J, Justinger C, Wagner M, Bohle RM, Kollmar O, Schilling MK, et al. Bronchobiliary fistula: a rare complication of hepatic endometriosis. Fertility and Sterility. 2011 Feb;95(2):804.e15–8. doi: 10.1016/j.fertnstert.2010.07.1087 37. Scioscia M, Pesci A, Scardapane A, Noventa M, Bonaccorsi G, Greco P, et al. Dye diffusion during laparoscopic tubal patency tests may suggest a lymphatic contribution to dissemination in endometriosis: A prospective, observational study. Laganà AS, editor. PLOS ONE. 2019 Dec 10;14(12):e0226264. doi: 10.1371/journal.pone.0226264 38. Seidler S, Shabanov S, Andres A, Karenovics W, Wenger J-M, Pluchino N. Diaphragmatic Endometriosis: Multidisciplinary Treatment. Journal of Minimally Invasive Gynecology. 2019 Mar;26(3):404. doi: 10.1016/j.jmig.2018.07.003 39. Sinder C, Dochat GR, Wentsler NE. Splenoendometriosis. American Journal of Obstetrics and Gynecology. 1965 Jul;92(6):883–4. doi: 10.1016/s0002-9378(16)34798-6 40. Takahashi R, Kurihara M, Mizobuchi T, Ebana H, Yamanaka S. Left-Sided Catamenial Pneumothorax with Thoracic Endometriosis and Bullae in the Alveolar Wall. Annals of Thoracic and Cardiovascular Surgery. 2017;23(2):108–12. doi: 10.5761/atcs.cr.16-00112 41. Thomakos N, Rodolakis A, Vlachos G, Papaspirou I, Markaki S, Antsaklis A. A Rare Case of Rectovaginal Endometriosis with Lymph Node Involvement. Gynecologic and Obstetric Investigation. 2006;62(1):45–7. doi: 10.1159/000091998 42. Tong S-S, Yin X-Y, Hu S-S, Cui Y, Li H-T. Case report of pulmonary endometriosis and review of the literature. Journal of International Medical Research. 2019 Mar 15;47(4):1766–70. doi: 10.1177/0300060518800868 43. Tuech J. Endometrial cyst of the liver: case report and review. Fertility and Sterility. 2003 May;79(5):1234–6. doi: 10.1016/s0015-0282(03)00178-x 44. Tulandi T, Sirois C, Sabban H, Cohen A, Murji A, Singh SS, et al. Relationship between Catamenial Pneumothorax or Non-catamenial Pneumothorax and Endometriosis. Journal of Minimally Invasive Gynecology. 2018 Mar;25(3):480–3. doi: 10.1016/j.jmig.2017.10.012 45. Ueki M. Histologic study of endometriosis and examination of lymphatic drainage in and from the uterus. American Journal of Obstetrics and Gynecology. 1991 Jul;165(1):201–9. doi: 10.1016/0002-9378(91)90252-m 46. Verbeke C, Hàrle M, Sturm J. Cystic Endometriosis of the Upper Abdominal Organs. Pathology - Research and Practice. 1996 Jan;192(3):300–4. doi: 10.1016/S0344-0338(96)80235-4 Рецензия Для цитирования: Украинец Р.В., Корнева Ю.С. Трансцеломическая и лимфо-гематогенная диссеминация эдометриоидных гетеротопий – механизм формирования экстрагенитальных форм эндометриоза. Журнал анатомии и гистопатологии. 2021;10(1):85-91. https://doi.org/10.18499/2225-7357-2021-10-1-85-91 For citation: Ukrainets R.V., Korneva Yu.S. Transcoelomic and Lympho-Hematogenous Dissemination of Endometrioid Heterotopias – the Mechanism of Extragenital Endometriosis Formation. Journal of Anatomy and Histopathology. 2021;10(1):85-91. (In Russ.) https://doi.org/10.18499/2225-7357-2021-10-1-85-91 JATS XML

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