Hum. Reprod. Advance Access originally published online on July 16, 2008
Human Reproduction 2008 23(10):2202-2209; doi:10.1093/humrep/den259
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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
1 Endometriosis Research Center Charité, Department of Gynecology, Charité, Campus Benjamin Franklin, Hindenburgdamm 30, 12200 Berlin, Germany 2 Institute of Pathology, Consultation and Reference Center for Lymph Node, Pathology and Hematopathology, Charité, Campus Benjamin Franklin, Hindenburgdamm 30 12200, Berlin, Germany
3 Correspondence address. E-mail: sylvia.mechsner{at}charite.de
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Abstract |
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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.
Key words: deep infiltrating endometriosis/sentinel lymph node/lymphatic spread/rectovaginal endometriosis/combined vaginal laparoscopic-assisted resection
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Introduction |
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Endometriosis is defined as chronic benign estrogen-dependent gynaecological disease that affects millions of women of reproductive age (Giudice and Kao, 2004
). Different forms of disease manifestations have been described such as endometriosis genitalis externa, adenomyosis uteri, endometriosis extragenitalis and deep infiltrating endometriosis (DIE).
The latter is characterized by the invasion of anatomical structures and organs by endometriotic foci and affects 
20–35% of women with endometriosis (Chapron et al., 2001; Chapron et al., 2003; Ford et al., 2004). DIE mainly involves the uterosacral ligaments, followed by the rectosigmoid colon, vagina and bladder. The estimated incidence of bowel endometriosis is between 5.3% and 12% (Macafee and Greer, 1960; Weed and Ray, 1987). The main location of bowel endometriosis is within the rectum and the rectosigmoid junction (Coronado et al., 1990; Bailey et al., 1994; Jerby et al., 1999). DIE of the rectovaginal septum is associated with dysmenorrhoea, deep dyspareunia, dyschezia, pelvic pain and infertility, causing significant reduction in quality of life (Fauconnier et al., 2002; Ford et al., 2004; Dubernard et al., 2006). Depending on depth of the infiltrative lesions within the bowel or adjacent organs, surgical excision of the deep infiltrating nodules is considered the most effective means of treatment (Garry et al., 2000; Chapron et al., 2001; Ford et al., 2004).
Although DIE is regarded as a benign disease, this specific form of endometriosis shows some similarities to malignant diseases such as infiltrating growth, damage of affected organs (bowel and vagina) and high recurrence rate (Thomas and Campbell, 2000). A recent study has demonstrated the presence of endometriosis in mesorectal lymph nodes (LNs) after bowel resection in cases of DIE. The incidence of endometriotic foci seems to be directly related to DIE extension (Abrao et al., 2006) and may be partially explained by the lymphatic spread of the disease (Noel et al., 2008). It is uncertain whether this observation is a local phenomenon or a sign of systemic disease.
The sentinel concept is well established in gynaecologic oncology, especially in vulva and breast cancer, but also starting in cervical and endometrial cancer (Altgassen et al., 2008). Pattern of lymphatic spread in the pelvis is a very complex process with different pathways (Reiffenstuhl, 1951; Plentl and Friedman, 1971). On the basis of our experience in patients with cervical cancer (Marnitz et al., 2006), we concluded that the lymphatic flow and the localization of the sentinel lymph nodes (SLNs) of the rectovaginal region must be similar.
The aim of our prospective study was to analyse the occurrence of endometriosis in pelvic SLN in patients with DIE.
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Materials and Methods |
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Patients
From May until December 2007, 14 patients underwent primary surgery for symptomatic palpable DIE. The selected patients had been suffering from dysmenorrhoea, deep dyspareunia, cyclic and acyclic pelvic pain as well as intestinal symptoms during menstruation such as painful defecation. The age of the patients ranged from 22 to 46 years (mean 32.6), 10 of those 14 patients had regular menstrual cycles without hormonal treatment, whereas four patients were taking oral contraceptives. Diagnosis of DIE was confirmed during surgery based on macroscopic appearance of the lesion using one or both of the following criteria: (i) palpable nodule or induration and (ii) dark blue nodule visible at the posterior vaginal wall.
A nerve sparing combined vaginal laparoscopic-assisted resection of the rectovaginal septum was performed. Depending on the depth of the endometriotic lesion within the bowel wall, segmental bowel resection was performed (Zanetti-Dallenbach et al., 2008). At the beginning of the surgery, 4 ccm Patent Blue® were injected around the visible and/or palpable nodule (Fig. 1A). During subsequent laparoscopy, the retroperitoneal space was opened lateral of the infundibulopelvic ligament, and blue coloured SLNs were removed from the iliac region (Fig. 1B and C) (Kohler et al., 2004; Marnitz et al., 2006) and examined by histology.
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We staged the disease during surgery, according to the revised American Society for Reproductive Medicine (1997)
with a rASRM stage: I = 1; II = 1; III = 4 and IV = 3. Additionally, we used the ENZIAN system (Tuttlies et al., 2005) for staging of the rectovaginal endometriosis and adenomyosis. In 13 patients, we detected an infiltration of the rectovaginal septum and also infiltration of one or more adjacent organs: large intestine (n = 11), vagina (n = 5), sacrouterine ligaments (n = 4) and ureter (n = 2). One patient had isolated adenomyosis uteri, a further five patients suffered from adenomyosis uteri in addition to other infiltrations. In 11 patients, segmental large bowel resection was performed with a length of 20–150 mm (mean 58 mm). Infiltration depth of the bowel wall was documented according to the deepest affected layer: the subserosa (n = 1), the stratum muscularis propria (n = 7) and the submucosal layer (n = 3).
According to DIE lesion size (graded intra- and post-operative by the surgeon) lesions were divided into four groups: <1 cm (n = 2); 1–2 cm (n = 4); 2–3 cm (n = 3); >3 cm (n = 4). Furthermore, DIE lesion site was classified according to the localization within the septum rectovaginale: right side (n = 5), left side (n = 0) and axial (n = 8) (Table I).
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The presence of endometrial glands and surrounding cytogenic stromal cells were taken as histological proof of DIE. Mesorectal LNs, incidentally discovered after bowel resection, were also submitted for histological examination.
All the surgically excised lesions were immediately fixed in buffered formalin 4% for 12 h and thereafter embedded in paraffin; 10–20 serial sections per patient of 1–2 µm thickness at five different levels of the SLN were immunohistochemically stained with antibodies against estrogen and progestogene receptors (ER and PR), CD10 and pan cytokeratin (CK). Some sections of the SLN were stained with haematoxylin and eosin (H&E). LNs that were incidentally found in the mesorectum after bowel resection were also examined. LNs of patients (age matched, 22–39 years) without evidence of endometriosis but of cervical cancer (n = 2; pelvine LN, removed for staging), large intestine diverticulitis (n = 5; mesorectal LN, concomitantly resected) or chronic infection of the nose-throat-region (n = 2, nuchal LN, excised for diagnostic purposes) were used as controls to give a spectrum of localizations.
The study was approved by the institutional review board of the Charité University Medical Center and all patients read and signed the informed-consent form.
Localization of the SLN
The localization of the SLN in the interiliac region was documented and divided into three groups: unilaterally right (n = 5), unilaterally left (n = 2) and bilaterally (n = 5) (Fig. 1C).
Immunohistochemistry
Estrogene (ER) and progestogene receptors (PR) analysis: after deparaffinization in Xylene [2 x 5 min at room temperature (RT)] and rehydration [10 min each at RT in Acetone, Acetone/Tris-buffered saline (TBS) (1:1) and TBS], heat induced epitope retrieval (HIER) procedure was performed by microwave cooking of probes in target buffer pH9 (Dako, Hamburg, Germany) at 700 W for 40 min. After rinsing with TBS, endogenous biotin was blocked with Biotin blocking solution (Dako). Then, fetal calf serum (FCS) was applied to minimize non-specific reactivities. Sections were incubated for 1 h at RT with monoclonal antibodies, recognizing estrogen or progestogene receptors (dilution 1:50, Dako). After rinsing with TBS, biotinylated anti-mouse immunoglobulin (IgG) (1:400) was applied for 40 min. In the final incubation step, streptavidin (1:400) (Roche, Germany) was applied for 40 min. Fuchsin-substrate (Dako) was used to visualize the specific immunoreactivity.
CK analysis: after deparaffinization and HIER procedure, probes were incubated with proteinase K (Dako). After rinsing with TBS, endogenous biotin was blocked with Biotin blocking solution (Dako). FCS was applied. Sections were incubated for 1 h at RT with a monoclonal antibody, recognizing CK5, 6, 8, 17 and 19 (clone MNF 116; dilution 1:100; Dako) and the staining was completed as described above.
CD10 analysis: after deparaffinization, HIER procedure was performed by cooking the probes in citrate buffer (0.1 M citric acid and 0.1 M sodiumcitrate, pH 6.0 at 700 W, microwave, 40 min). After rinsing with TBS, endogenous biotin was blocked with Biotin blocking solution (Dako). FCS was applied. Sections were incubated for 1 h at RT with a monoclonal antibody, recognizing CD10 (dilution 1:80, Novocastra, Newcastle, UK). After rinsing with TBS, biotinylated anti-mouse immunoglobulin (IgG) (1:400) was applied for 40 min and the same procedure was performed to visualize the specific immunoreactive staining.
Ki-67 analysis: analysis was performed using the primary antibodies against Ki-67 (clone MIB-1, dilution 1:2000), obtained from Dako. Detection was done using the alkaline-phosphatase anti-alkaline phosphatase complex (APAAP) method with Fast Red as chromogen.
Negative control sections were processed by using non-specific IgG (dilution 1:50; Dako) and by omitting the specific primary antibody. Endometrium of non-pregnant women was used as positive control.
Staining was detected using an axiophot (Carl Zeiss, Göttingen, Germany) microscope. Photomicrographs were taken at different magnifications (x40 and x100) and were further processed using Adobe Photoshop (Adobe Systems, Unterschleissheim, Germany).
Immunohistochemical evaluation of the LN
When an endometriotic lesion was detected, its signal intensity of ER, PR and Ki67 staining was graded according to the percentage of nuclear staining of the cells. CD10 and CK were documented as positive staining (in stromal and epithelial cells of the endometriotic lesion) without additional grading. Of each SLN, 10–20 sections out of five different LN levels were analysed.
Furthermore, all LNs were analysed according to their anatomical structures in the subcapsular sinus, the superficial cortex and in the medulla. Occurrence of disseminated ER/PR positive cells was graded: + = <50 cells, ++ = 50–150 cells, and +++ = >150 cells for each LN region. The precise distribution of ER/PR positive cells in the specific anatomical structures of the LNs was documented (S, subcapsular sinus; C, superficial cortex and M, medulla).
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Results |
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SLN detection and localization
In all patients, DIE was confirmed by histology. In 11 out of 13 patients with DIE and in one patient with adenomyosis uteri, blue coloured SLNs were detected at the time of laparoscopy and removed. The SLNs were unilateral in 7 of 12 patients (58.3%) and bilateral in 5 of 12 patients (41.7%). Overall, 18 SLNs were removed. The localization of SLN followed the typical LN spread of the upper vagina.
We observed a higher frequency of bilateral localization with increasing size of DIE lesion (Table I).
Immunohistochemical analysis of the SLN
Endometriotic lesions in SLN
In 4 of 18 SLNs (22.2%) from 3 of 12 patients (25%), we found typical endometriotic lesions with epithelial glands and surrounding cytogenic stromal cells. Immunohistological analysis showed that both epithelial and stromal cells expressed ER (100%/95%) and PR (100%). CD10 and CK expression was also positive (Fig. 2A–F).
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Disseminated ER and PR positive cells in SLNs
In addition to histologically defined endometriotic lesions, we also observed single disseminated cells interspaced in the LN tissue. In 10 of 12 patients (83.3%) or in 16 of 18 (88.9%) SLNs, disseminated PR positive cells were detected. Also, in 7 of 12 patients (58.3%) or in 9 of 18 (50%) SLNs, disseminated ER positive cells were identified. Disseminated ER/PR positive cells were mainly located in the subcapsular sinuses, the superficial cortex and the medulla of the LN (Fig. 2E–H) and were negative for CD10 and CK. The surrounding capsule was intact in all LNs examined. The disseminated ER/PR positive cells were located intranodular.
Only few single CD10 and CK positive cells were detected in the medulla but the staining pattern was similar to control LN of patients without endometriosis, equivalent to the known distribution of these markers in normal LN (Chan et al., 2000; Cook et al., 2003). However, no ER and PR positive cells were detectable in control LN.
Immunohistochemical analysis of incidental LN
We also investigated two incidental mesorectal LN in patients with segmental bowel resection. One of them showed an endometriotic lesion with ER/PR/CK/CD10 reactivity and an increased number of disseminated PR/ER positive cells in the subcapsular sinuses, superficial cortex and the medulla of the LN. The other LN did not display any endometriotic lesions, which was confirmed by lack of detectable immunoreactivity for the aforementioned markers.
Expression of Ki67 in SLNs and incidental LNs
Ki67 staining demonstrated a similar expression pattern in all investigated LNs. In the endometriotic lesions, Ki67 staining was detectable. Ki67 expression was seen in 5–10% of epithelial and stromal cells. Disseminated ER/PR positive cells showed no proliferative activity by Ki67.
Occurrence of endometriostic lesions and ER/PR positive cells in relation to the size of the DIE
The number and the occurrence of disseminated ER/PR positive cells appear to be correlated with the size of the DIE lesion (Tables II and III): the larger the size of the primary DIE lesions, the greater the number of disseminated endometriotic cells and endometriotic foci in the SLN to be detected.
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Discussion |
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The surgical excision of the deep infiltrating nodules is considered the most effective treatment (Garry et al., 2000
; Chapron et al., 2001) with an estimated recurrence rate of 13–15% (Varol et al., 2003; Ford et al., 2004). However, colorectal resection for endometriosis may be associated with major complications including rectovaginal fistula and digestive symptoms such as chronic constipation or diarrhoea.
In order to reduce these complications (Possover et al., 2000), a nerve and tissue sparing technique with segmental resection of the bowel tube but preservation of the mesorectum was developed (Zanetti-Dallenbach et al., 2008). All patients in this study underwent this surgical technique. As a consequence of tissue-restricted excision, only two incidental LNs were found in the mesorecal tissue in cases of bowel resection.
The LN involvement in patients with endometriosis is a new aspect of this complex disease. Currently only limited information is available regarding the role of LNs. One reason may be the ‘surgical principle’ that LN dissection is only performed in staging procedures for malignant diseases. There are only two studies and a few case reports regarding the regional LN involvement of the mesocolon in patients with bowel resection for rectosigmoid endometriosis (Abrao et al., 2006; Thomakos et al., 2006; Barrier et al., 2007; Noel et al., 2008). A recent study of 35 patients with DIE demonstrated 19 incidental LNs in the mesorectal resection specimens. In five patients, endometriosis was identified by H&E staining. The percentage of endometriotic lesions in these LNs seemed to be proportional to the volume of the endometriotic lesion (Abrao et al., 2006). Furthermore, other authors demonstrated frequent mesorectal LN involvement by endometriotic foci in rectosigmoid endometriosis, probably resulting from its lymphatic spread (Noel et al., 2008).
Currently, it is unclear whether this observation is a local phenomenon or a sign of systemic disease. We demonstrated for the first time the presence of SLN in the interiliac area of patients with DIE, comparable with the topographic distribution of SLN in patient with cervical cancer (Marnitz et al., 2006). This strategy of SLN detection using Patent Blue is based on encouraging results seen in patients with cervical cancer (Altgassen et al., 2008). The SLN concept postulates that this SLN is the first one draining a defined anatomic region. The histologic evaluation of the SLN may be informative with regard to the ‘metastasis formation’ potential of the underlying disease (Torne and Puig-Tintore, 2004; Marnitz et al., 2006).
In 12/14 patients (85.7%), we detected SLN in the interiliac region. The SLNs were unilaterally located in 58.3% and bilaterally located in 41.7% of patients. However, it is unclear whether this distribution pattern is due to anatomic variations or is related to the lesion size (Reiffenstuhl, 1951). A possible contributing factor for this finding seems to be the size of the lesion. In the majority of patients with a lesion diameter of >2 cm, LNs were detected bilaterally.
In addition to routine H&E staining, immunohistochemical testing for ER and PR was performed in order to identify endometriotic cells, which often express these receptors (Fujishita et al., 1997). Furthermore, immunohistochemical analysis for CD10, an endometrial stromal cell marker (Sumathi and McCluggage, 2002; Onda et al., 2003) and pan CK, an epithelial cell marker, was performed. In three patients (25%), endometriotic lesions were identified by H&E staining in four SLNs of the interiliac region. These lesions were positive for ER/PR, CK and CD10. However, by using immunohistochemical staining, disseminated ER/PR positive cells were identified in 83.3% of the patients. These disseminated cells were negative for CD10 and CK. A possible explanation for this discrepancy could be that differentiation of these disseminated ER/PR positive cells into endometriotic-like epithelial cells and stromal cells was induced by metaplasia in an ongoing process. In the case of endometriotic lesion with glandular epithelial cells and stromal cells in tissue formation, all four markers for endometriosis were positive.
Another explanation could be the natural occurrence of ER/PR positive cells. However, the control LN of female patients without endometriosis did not show such a cell population. In order to compare LN of patients affected by endometriosis with patients without a systemic disease, we chose LN of patients without cancer.
Another possibility is that these cells are some kind of immune cells. Reviewing the recent literature did not support this hypothesis and a similar cell population with this receptor profile in LN has not been described up to now in humans. These endometriotic-like cells have to be characterized in more detail in the near future.
In addition, the occurrence and the number of disseminated ER/PR positive cells, as well as the typical endometriotic lesions in SLN, were analysed. Our results (Tables II and III) suggested the larger the primary DIE lesion, the higher the number of disseminated endometriotic-like cells and endometriotic foci in the SLN.
In agreement with other authors, we found endometriotic lesions in regional mesorectal LN (Abrao et al., 2006; Noel et al., 2008). In contrast to these results, we detected furthermore disseminated ER and PR positive cells in the subcapsular sinuses and superficial cortex of the LN.
Our investigation supports the hypothesis for lymphatic spread of endometriotic cells from the upper part of the vagina, with the distinct potential of this specific type of endometriosis for systemic processes. However, the biological importance of this phenomenon is currently not fully understood. The term ‘metastasis’ is reserved for the displacement of tumour cells in malignant disease to a region distant to the primary tumour. However, typical markers for metastasing potential such as the persistence of non-differentiated cells in the subcapsular sinuses, the superficial cortex and the medulla of LN as well as the formation of tissue with proliferative activity can be found in endometriosis as well.
On the other hand, we found an intact capsule and disseminated cells only in the intranodular compartment in all patients. Furthermore, all endometriotic foci lacked nuclear atypia, abnormal mitotic activity or increased nuclear-to-cytoplasmatic ratio, criteria typical for malignancy (Barrier et al., 2007). Thus displaced endometriotic foci have to be differentiated from metastatic spread in malignancies. Disseminated ER/PR positive cells may have the potential to develop into a fully differentiated endometriotic lesion composed of epithelial glands and surrounding cytogenic stromal cells.
This process may be controlled by the immune system, and LN involvement may indicate chronic manifestation of endometriosis with a high recurrence rate.
DIE shows similarities to malignant diseases such as infiltrating growth and destruction of affected organs. Furthermore, several authors reported the potential for malignant transformation of endometriotic lesions (Zanetta et al., 2000; Ulrich et al., 2003). However, malignant transformation of DIE appears to be rare (Brooks and Wheeler, 1977; Berger et al., 2001; Ulrich et al., 2005). In addition, the localization of recurrent endometriosis in LN has not been reported, although this does not exclude that LN may act as a reservoir for recurrent or chronic disease.
Our results pose a list of questions regarding the extent of radical surgery. Is it justifiable to limit the surgical resection to the infiltrated bowel with or without mesocolon? or Is a more extended approach warranted with additional removal of the regional LN as well as of the LN of the iliac region such as in malignancy? Possibly, tissue-sparing surgery combined with SLN removal can be beneficial for the patients.
In summary, the results of this pilot study highlighted the occurrence of ER and PR positive endometriotic lesions and disseminated cells in pelvic SLN of patients with DIE. The disseminated cells may be part of a differentiation process which leads to the formation of endometriotic lesions by metaplasia. Our work will be extended to ascertain the biological importance of the persistence of endometriotic- and endometriotic-like cells in LN and its therapeutical consequences.
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Acknowledgement |
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The authors are grateful to Giovanni Favero MD and Johanna Herbel PhD for fruitful discussions and to Arwed Mechsner for his valuable technical assistance with the picture preparation.
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References |
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Submitted on March 4, 2008; resubmitted on April 30, 2008; accepted on June 2, 2008.
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