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

Abstract

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.

Fig 1. Laparoscopic images.

A scattered blue area (arrow) after a dye test (A) that was biopsied (B).

Fig 2. Laparoscopic images during a tubal dye test.

The uterus showed a transient scattered blue color and unilateral right tubal permeability was demonstrated (A). A deep blue color of the endometriosis nodule of the right uterosacral ligament appeared after a few seconds (B) along with a progressive staining of lymphatic vessels of the infundibulopelvis ligament (C). A blue spot was seen where lymph nodes of the internal iliac vein lie (D).

Fig 3. Laparoscopic images.

The photo sequence (A to D) shows the methylene blue solution that seeped through the tubes and that permeated the uterine wall (A); after a short while, only sub-perimetrial vessels remained dyed (B) and a few seconds later, a clear staining of the lymphatics surrounding di utero-ovarian artery and vein was evident (C). The dye took some minutes to reach the ovary that showed a faint blue color of the cortex beneath the tunica albuginea (D). Photo E shows an endometriosis lesion within a lymphatic vessel of the lateral abdominal wall (the inset at the lower right corner shows a higher magnification thereof) as demonstrated at immunohistochemistry. Two endometriosis foci deeply invaded the peritoneum that lined the right diaphragm (F).

Fig 4. Laparoscopic and histologic images.

Clustered areas of the uterus were permeated by the methylene blue during a dye test that showed bilateral permeability of the tubes (A). After opening the peritoneum of the anterior broad ligament, a blue staining of the connective tissue beneath the round ligament (*) was found (B). In this case, a deep biopsy of the uterine wall where the color changed was taken and adenomyosis with ectatic lymphatic vessels was demonstrated. Deparaffinized 4-μm sections were immunostained with antibodies against CD34 and podoplanin (C and D, respectively) to confirm that the ectatic vessels were lymphatics.

Fig 5. Laparoscopic images.

An apparently normal uterus (A) shaded into a peculiar blue color during a methylene blue test in a case of diffuse adenomyosis (C). Bilateral tubal permeability was demonstrated (B).