Dye diffusion during laparoscopic tubal patency tests may suggest a lymphatic contribution to dissemination in endometriosis: A prospective, observational study


Autoři: Marco Scioscia aff001;  Anna Pesci aff003;  Arnaldo Scardapane aff004;  Marco Noventa aff002;  Gloria Bonaccorsi aff005;  Pantaleo Greco aff005;  Giuseppe Zamboni aff003
Působiště autorů: Department of Obstetrics and Gynecology, Sacro Cuore Don Calabria Hospital, Negrar, Verona, Italy aff001;  Department of Obstetrics and Gynecology, Policlinico Hospital, Abano Terme, Padua, Italy aff002;  Department of Pathology, Sacro Cuore Don Calabria Hospital, Negrar, Verona, Italy aff003;  Interdisciplinary Department of Medicine, Section of Radiology, University of Bari Medical School, Bari, Italy aff004;  Department of Morphology, Surgery and Experimental Medicine, Section of Obstetrics and Gynecology, University of Ferrara, S. Anna University Hospital, Cona, Ferrara, Italy aff005
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226264

Souhrn

Aim

Women with adenomyosis are at higher risk of endometriosis recurrence after surgery. This study was to assess if the lymphatic vessel network drained from the uterus to near organs where endometriosis foci lied.

Methods

A prospective, observational study, Canadian Task Force Classification II-2, was conducted at Sacro Cuore Don Calabria Hospital, Negrar, Italy. 104 white women aged 18–43 years were enrolled consecutively for this study. All patients underwent laparoscopy for endometriosis and a tubal dye test was carried out.

Results

Evidence of dye dissemination through the uterine wall and outside the uterus was noted in 27 patients (26%) with adenomyosis as it permeated the uterine wall and a clear passage of the dye was shown in the pelvic lymphatic vessels regardless whether the tubes were unobstructed. Histological assessment of the uterine biopsies confirmed adenomyosis.

Conclusion

Adenomyosis is characterized by ectatic lymphatics that allow the drainage of intrauterine fluids (the dye and, perhaps, menstrual blood) at minimal intrauterine pressure from the uterine cavity though the lymphatic network to extrauterine organs. Certainly, this may not be the only explanation for endometriosis dissemination but the correlation between the routes of the dye drainage and location of endometriosis foci is highly suggestive.

Klíčová slova:

Biopsy – Histology – Laparoscopy – Ligaments – Surgical and invasive medical procedures – Uterus – Myometrium – Gynecologic surgery


Zdroje

1. Practice Committee of the American Society for Reproductive Medicine. Endometriosis and infertility: a committee opinion. Fertil Steril. 2012;98(3):591–8. doi: 10.1016/j.fertnstert.2012.05.031 22704630

2. Giudice Linda C., Kao Lee C. Endometriosis. Lancet Lond Engl. 2004;364(9447):1789–99.

3. Guerriero S, Saba L, Pascual MA, Ajossa S, Rodriguez I, Mais V, Alcazar JL. Transvaginal ultrasound vs magnetic resonance imaging for diagnosing deep infiltrating endometriosis: systematic review and meta-analysis. Ultrasound Obstet Gynecol. 2018;51(5):586–595. doi: 10.1002/uog.18961 29154402

4. Fratelli N, Scioscia M, Bassi E, Musola M, Minelli L, Trivella G. Transvaginal sonography for preoperative assessment of deep endometriosis. J Clin Ultrasound. 2013;41(2):69–75. doi: 10.1002/jcu.22018 23233390

5. Scioscia M, Orlandi S, Trivella G, Portuese A, Bettocchi S, Pontrelli G, et al. Sonographic differential diagnosis in deep infiltrating endometriosis: The bowel. Biomed Research Internat, 2019, Vol. 2019, Article ID 5958402, https://doi.org/10.1155/2019/5958402

6. Laganà AS, Vitale SG, Granese R, Palmara V, Ban Frangez H, Vrtacnik-Bokal E, et al. Clinical dynamics of Dienogest for the treatment of endometriosis: from bench to bedside. Expert Opin Drug Metab Toxicol. 2017;13(6):593–596. doi: 10.1080/17425255.2017.1297421 28537213

7. Minelli L, Ceccaroni M, Ruffo G, Bruni F, Pomini P, Pontrelli G, et al. Laparoscopic conservative surgery for stage IV symptomatic endometriosis: short-term surgical complications. Fertil Steril. 2010;94(4):1218–22. doi: 10.1016/j.fertnstert.2009.08.035 19969292

8. Raffaelli R, Garzon S, Baggio S, Genna M, Pomini P, Laganà AS, et al. Mesenteric vascular and nerve sparing surgery in laparoscopic segmental intestinal resection for deep infiltrating endometriosis. Eur J Obstet Gynecol Reprod Biol. 2018; 231:214–219. doi: 10.1016/j.ejogrb.2018.10.057 30415128

9. Laganà AS, Vitale SG, Trovato MA, Palmara VI, Rapisarda AM, Granese R, et al. Full-Thickness Excision versus Shaving by Laparoscopy for Intestinal Deep Infiltrating Endometriosis: Rationale and Potential Treatment Options. Biomed Res Int. 2016;2016:3617179. doi: 10.1155/2016/3617179 27579309

10. Ceccaroni M, Clarizia R, Alboni C, Ruffo G, Bruni F, Roviglione G, et al. Laparoscopic nerve-sparing transperitoneal approach for endometriosis infiltrating the pelvic wall and somatic nerves: anatomical considerations and surgical technique. Surg Radiol Anat. 2010;32(6):601–4. doi: 10.1007/s00276-010-0624-6 20087591

11. Stepniewska A, Pomini P, Scioscia M, Mereu L, Ruffo G, Minelli L. Fertility and clinical outcome after bowel resection in infertile women with endometriosis. Reprod Biomed Online. 2010;20(5):602–9. doi: 10.1016/j.rbmo.2009.12.029 20359953

12. Scioscia M, Bruni F, Ceccaroni M, Steinkasserer M, Stepniewska A, Minelli L. Distribution of endometriotic lesions in endometriosis stage IV supports the menstrual reflux theory and requires specific preoperative assessment and therapy. Acta Obstet Gynecol Scand. 2011;90(2):136–9. doi: 10.1111/j.1600-0412.2010.01008.x 21241258

13. Koninckx PR, Ussia A, Adamyan L, Wattiez A, Donnez J. Deep endometriosis: definition, diagnosis, and treatment. Fertil Steril. 2012;98(3):564–71. doi: 10.1016/j.fertnstert.2012.07.1061 22938769

14. Davis A, Goldberg J. Extrapelvic Endometriosis. Semin Reprod Med. 2016;35(01):098–101.

15. Vercellini P, Viganò P, Somigliana E, Fedele L. Endometriosis: pathogenesis and treatment. Nat Rev Endocrinol. 2014;10(5):261–75. doi: 10.1038/nrendo.2013.255 24366116

16. Jerman LF, Hey-Cunningham AJ. The Role of the Lymphatic System in Endometriosis: A Comprehensive Review of the Literature. Biol Reprod. 2015;92(3).

17. Sheveleva T, Bejenar V, Komlichenko E, Dedul A, Malushko A. Innovative approach in assessing the role of neurogenesis, angiogenesis, and lymphangiogenesis in the pathogenesis of external genital endometriosis. Gynecol Endocrinol Off J Int Soc Gynecol Endocrinol. 2016;32(sup2):75–9.

18. Struble J, Reid S, Bedaiwy MA. Adenomyosis: A Clinical Review of a Challenging Gynecologic Condition. J Minim Invasive Gynecol. 2016;23(2):164–85. doi: 10.1016/j.jmig.2015.09.018 26427702

19. García-Solares J, Donnez J, Donnez O, Dolmans MM. Pathogenesis of uterine adenomyosis: invagination or metaplasia? Fertil Steril. 2018;109(3):371–9. doi: 10.1016/j.fertnstert.2017.12.030 29566849

20. Ueki M. Histologic study of endometriosis and examination of lymphatic drainage in and from the uterus. Am J Obstet Gynecol. 1991;165(1):201–9. doi: 10.1016/0002-9378(91)90252-m 1853897

21. Ceccaroni M, Clarizia R, Bruni F, D'Urso E, Gagliardi ML, Roviglione G, et al. Nerve-sparing laparoscopic eradication of deep endometriosis with segmental rectal and parametrial resection: the Negrar method. A single-center, prospective, clinical trial. Surg Endosc. 2012;26(7):2029–45. doi: 10.1007/s00464-012-2153-3 22278102

22. Ansari AH. Methylene blue test for assessment of tubal patency: a new and simple technique. Can Med Assoc J. 1968;99(4):182–44. 5317820

23. Jeng CJ., Huang SH., Shen J, Chou CS., Tzeng CR. Laparoscopy-guided myometrial biopsy in the definite diagnosis of diffuse adenomyosis. Hum Reprod. 2007;22(7):2016–9. doi: 10.1093/humrep/dem084 17428879

24. Sampson JA. Ovarian hematomas of endometrial type (perforating hemorrhagic cysts of the ovary) and implantation adenomas of endometrial type. Boston Med Surg J. 1922;186:445–56.

25. Laganà AS, Vitale SG, Salmeri FM, Triolo O, Ban Frangez H, Vrtacnik-Bokal E, et al. Unus pro omnibus, omnes pro uno: A novel, evidence-based, unifying theory for the pathogenesis of endometriosis. Med Hypotheses. 2017;103:10–20. doi: 10.1016/j.mehy.2017.03.032 28571791

26. Laganà AS, Salmeri FM, Vitale SG, Triolo O, Götte M. Stem Cell Trafficking During Endometriosis: May Epigenetics Play a Pivotal Role? Reprod Sci. 2018;25(7):978–979. doi: 10.1177/1933719116687661 28100109

27. Benagiano G, Brosens I, Habiba M. Adenomyosis: a life-cycle approach. Reprod Biomed Online. 2015;30(3):220–32. doi: 10.1016/j.rbmo.2014.11.005 25599903

28. Di Donato N, Montanari G, Benfenati A, Leonardi D, Bertoldo V, Monti G, et al. Prevalence of adenomyosis in women undergoing surgery for endometriosis. Eur J Obstet Gynecol Reprod Biol. 2014;181:289–93. doi: 10.1016/j.ejogrb.2014.08.016 25201608

29. Tellum T, Nygaard S, Lieng M. Noninvasive Diagnosis of Adenomyosis: A Structured Review and Meta-Analysis of Diagnostic Accuracy in Imaging. J Minim Invasive Gynecol. 2019, S1553-4650(19)31287-7

30. Van den Bosch T, Van Schoubroeck D. Ultrasound diagnosis of endometriosis and adenomyosis: State of the art. Best Pract Res Clin Obstet Gynaecol. 2018; 51:16–24. doi: 10.1016/j.bpobgyn.2018.01.013 29506961

31. Vercellini P, Frontino G, Pietropaolo G, Gattei U, Daguati R, Crosignani PG. Deep endometriosis: definition, pathogenesis, and clinical management. J Am Assoc Gynecol Laparosc. 2004;11(2):153–61. doi: 10.1016/s1074-3804(05)60190-9 15200766

32. Javert C. T. Pathogenesis of endometriosis based on endometrial homeoplasia, direct extension, exfoliation and implantation, lymphatic and hematogenous metastasis, including five case reports of endometrial tissue in pelvic lymph nodes. Cancer. 1949;2(3):399–410. doi: 10.1002/1097-0142(194905)2:3<399::aid-cncr2820020304>3.0.co;2-l 18131400

33. Benagiano G, Brosens I, Habiba M. Structural and molecular features of the endomyometrium in endometriosis and adenomyosis. Hum Reprod Update. 2014;20(3):386–402. doi: 10.1093/humupd/dmt052 24140719

34. Landi S, Mereu L, Pontrelli G, Stepniewska A, Romano L, Tateo S, et al. The Influence of Adenomyosis in Patients Laparoscopically Treated for Deep Endometriosis. J Minim Invasive Gynecol. 2008;15(5):566–70. doi: 10.1016/j.jmig.2008.06.009 18722969

35. Machairiotis N, Stylianaki A, Dryllis G, Zarogoulidis P, Kouroutou P, Tsiamis N, et al. Extrapelvic endometriosis: a rare entity or an under diagnosed condition? Diagn Pathol. 2013;8(1):194.

36. Gungor T, Kanat-Pektas M, Ozat M, Zayifoglu Karaca M. A systematic review: endometriosis presenting with ascites. Arch Gynecol Obstet. 2011;283(3):513–8. doi: 10.1007/s00404-010-1664-1 20821226

37. Scioscia M, Scardapane A, Ceccaroni M. Regarding “Continuous Amenorrhea May be Insufficient to Stop the Progression of Colorectal Endometriosis.” J Minim Invasive Gynecol. 2016;23(7):1203–5. doi: 10.1016/j.jmig.2016.06.010 27329546

38. Netter A, d'Avout-Fourdinier P, Agostini A, Chanavaz-Lacheray I, Lampika M, Farella M, et al. Progression of deep infiltrating rectosigmoid endometriotic nodules. Hum Reprod. 2019: dez188. doi: 10.1093/humrep/dez188 31687764

39. Cho S, Choi YS, Yun BH, Chon SJ, Jung YS, Kim H, et al. Effects of Levonorgestrel-Releasing Intrauterine System on Lymphangiogenesis of Adenomyosis. Am J Clin Pathol. 2015;143(3):352–61. doi: 10.1309/AJCPP8F4SFYFVXRN 25696793

40. Restaino S, Ronsini C, Finelli A, Perrone E, Scambia G, Fanfani F. Role of blue dye for sentinel lymph node detection in early endometrial cancer. Gynecol Surg. 2017;14(1):23. doi: 10.1186/s10397-017-1026-0 29213225

41. Laganà AS, Garzon S, Franchi M, Casarin J, Gullo G, Ghezzi F. Translational animal models for endometriosis research: a long and windy road. Ann Transl Med. 2018;6(22):431. doi: 10.21037/atm.2018.08.24 30596061

42. Barra F, Scala C, Mais V, Guerriero S, Ferrero S. Investigational drugs for the treatment of endometriosis, an update on recent developments. Expert Opin Investig Drugs. 2018;27(5):445–458. doi: 10.1080/13543784.2018.1471135 29708812


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