High prevalence of endometriosis in infertile women with normal ovulation and normospermic partners

12 11 2009

To the Editor:

We read the article by Meuleman et al. (1) with interest. The high incidence of endometriosis (47%) and other pelvic pathology (29%) in this cohort makes a strong case for offering laparoscopy and hysteroscopy to couples with “unexplained infertility” (a diagnosis of exclusion). This diagnosis however requires confirmation of tubal integrity, and the issue is whether laparoscopy should be the first-line investigation to establish tubal patency. The authors did not say how many women in their cohort had a completely normal pelvis following laparoscopy and hysteroscopy.

Their data, put in another way, showed that 53% of the women who under went laparoscopy did not have endometriosis. It is in an effort to minimize the risks and costs associated with laparoscopy that NICE (2) recommends that hysterosalpingogram be considered as the first-line test for tubal patency, and laparoscopy be considered only for women with “co-morbidity.” Although the definition of co-morbidity is fairly non-specific, it generally refers to women whose clinical history may suggest the presence of potential pelvic pathology. This includes those who have had previous pelvic infection, previous ectopic pregnancy, known endometriosis, etc. By limiting laparoscopy to this cohort, fewer women are exposed to the risks associated with this procedure and its potential cost implications.

Also, as interesting as it is to know that laparoscopy revealed a high incidence of endometriosis and other “fertility-reducing pathologies” among the cohort of women studied, the authors failed to discuss the outcome of the treatment of these pathologies. We must never lose sight of the fact that the ultimate aim of infertile women undergoing any type of treatment is to take home a baby. Until this is achieved, the patients may be thankful for having their asymptomatic endometriosis resected, but will remain dissatisfied and consider the treatment a failure should they not have a baby at the end. It will be interesting to know how many women had a live birth following surgery in this cohort.

Krithiga Ilangavan, MRCOG
Kingston Hospital NHS Trust
Kingston Upon Thames, United Kingdom

Emmanuel Kalu, MRCOG
Assisted Concepton Unit
Queen Mary’s Hospital
London, United Kingdom

References
1. Meulemann C, Vandenabeele B, Fieuws S et al. High Prevalence of endometriosis in infertile women with normal ovulation and normospermic partners. Fertil Steril 2009, 92;1:68-74.

2. National Collaboration Centre for Women’s and Children’s Health. Clinical Guideline 11:fertility: assessment and treatment for people with fertility problems. UK, NICE, 2004.

Published online in Fertility and Sterility doi:10.1016/j.fertnstert.2009.11.027

Endometriosis: Is laparoscopy justified without previous ultrasonogram and MRI?

To the Editor:

In the article by Meuleman et al. (1), I appreciated the new understandings brought by the authors and the unexpected demonstration that pelvic pain was not explained by the existence of endometriotic lesions in 46% of cases in infertile women.

Nevertheless, I am surprised about the last sentence of their abstract, “Reproductive surgery is indicated in infertile women belonging to the study population….” Nothing in the article supports this assertion, neither the statistical results nor the references. However, the following criticisms are more important:

1) Whereas so many details are credited to the expertise of the surgical team, nothing is mentioned about the ultrasonographer’s competence. Still d’Hooghe and Timmerman themselves had written that the results of ultrasonograms are dependent on the experience and interest of the ultrasonographer (2). The progress made in discovering nodular lesions of endometriosis and the abnormal position of pelvic organs due to adhesions, when the ultrasonographer is talented, cannot be ignored.

2) Magnetic resonance imaging (MRI) is never mentioned. Even if the team does not have access to the necessary equipment, the information contributed by this technique is so well recognized (3) that it should have been mentioned, since the indications for surgery with its possible side effects are not the same if the lesions discovered necessitate it or if they might just be improved by surgery.

3) More surprisingly, the existence or absence in the patients of adenomyosis associated with endometriosis was never mentioned in work from a team that has written a remarkable article on adenomyosis and infertility (2). It is possible that the diagnosis of adenomyosis being difficult for the ultrasonographer, and as no MRI had been used, the authors decided not to raise the question, but this deficiency seriously affects the conclusions of the work, as the internal adenomyotic lesions are not accessible to laparoscopic surgery! Nevertheless, as hysteroscopy was a mandatory part of the investigations, it is difficult to understand that a possible role of adenomyotic lesions has never been at least hypothesized.

Bearing in mind all these uncertainties, it appears that the conclusions in the article are at least too abrupt, as authors insist on the advantages of surgery, which is today subject of discussion because its dangers have been hidden for such a long time and because the progress of MRI and ultrasonography are now well established, in parallel with the good results of assisted reproductive technology. In the August issue of Fertility and Sterility, Chapron et al. have written, “When the clinical examination (questioning and pelvic exam) suggests deep infiltrating endometriosis we feel that the first additional investigation should be transvaginal ultrasonography. In this context, the discovery of an ovarian endometrioma at transvaginal ultrasonography should prompt the practitioner to search for severe lesions (intestinal and/or ureteral involvement) rather than programming surgery immediately.” (4).

It will be a pleasure if the authors’ reply shows that my criticisms were unjustifiably excessive.

Jean Belaisch, M.D.
Department of Gynaecology and Obstetrics
Saint Vincent de Paul Hospital
Paris, France

References
1. Meuleman C, Vandenabeele B, Fieuws S, Spiessens C, Timmerman D, D’Hooghe T. High prevalence of endometriosis in infertile women with normal ovulation and normospermic partners. Fertil Steril. 2009 Jul;92(1):68-74.

2. Devlieger R, D’Hooghe T, Timmerman D. Uterine adenomyosis in the infertility clinic. Hum Reprod Update. 2003 Mar-Apr;9(2):139-47.

3. Kunz G, Beil D, Huppert P, Noe M, Kissler S, Leyendecker G. Adenomyosis in endometriosis–prevalence and impact on fertility. Evidence from magnetic resonance imaging. Hum Reprod. 2005 Aug;20(8):2309-16.

4. Chapron C , Pietin-Vialle C , Borghese B, Davy C, Foulot H, Chopin N. Associated ovarian endometrioma is a marker for greater severity of deeply infiltrating endometriosis. Fertil Steril 2009 Aug ; 92(2): 453-57.

Published online in Fertility and Sterility doi:10.1016/j.fertnstert.2009.11.026

The Authors Respond:

We thank colleagues Belaisch, Ilangavan and Kalu for their interest in our work (1).

Our conclusion that reproductive surgery is indicated in infertile women with regular menstrual cycles whose male partners have normal sperm quality is justified. Firstly, significant pelvic (including endometriosis), tubal or uterine pathology was observed in 2/3 of our patients and can be interpreted as significant comorbidity and justification for surgery according to the NICE guidelines (2). Secondly, a completely normal hysteroscopy and laparoscopy were only observed in 1/3 of our patients (1), but in this “normal” group diagnostic hysteroscopy and laparoscopy can still be clinically justified to confirm the diagnosis of unexplained infertility, since a normal hysterosalpingography does not exclude significant pelvic pathology (3).

Although a lot of progress has been made in the ultrasound diagnosis of endometriosis with respect to ovarian endometriotic cysts and nodular lesions in the rectovaginal area, and both experience and interest of the ultrasonographer are important in the diagnosis of adenomyosis (4), ultrasound is not reliable in the diagnosis or exclusion of pelvic peritoneal endometriosis found in women with minimal to mild endometriosis (5). Furthermore, some endometriotic nodules are situated higher in the rectosigmoidal area, which is not routinely accessible by transvaginal ultrasound. Finally, the retrospective nature of our study and the variable interval between preoperative ultrasound and surgery may have diluted the diagnostic value of ultrasound in this study. This aspect will be taken care of in our ongoing prospective cohort study.

We disagree with Dr Belaisch that hysteroscopy is useful for the diagnosis of endometriosis (no published data supporting this statement) or that magnetic resonance imaging (MRI) is needed for the diagnosis of adenomyosis, as several studies have shown that ultrasound diagnosis of adenomyosis is as reliable as MRI diagnosis (4-6). Adenomyosis was not a relevant issue in our study for the following reasons: Firstly, the relationship between adenomyosis and infertility is not properly quantified; secondly, adenomyosis cannot be treated by surgery or by medication in women who want to become pregnant. Therefore, in our study, adenomyosis was not a factor of importance in deciding for or against surgery.

Clearly, MRI is not a first-line investigation in this study population of infertile women whose husbands have normal sperm (5). MRI or other imaging techniques like intravenous pyelogram or bowel contrast radiography are indicated and used in our center when more extensive endometriosis with impact on bowel, bladder and/or ureter is suspected based on clinical examination and ultrasound imaging (5, 7). Furthermore, based on randomized controlled trials, excisional endometriosis surgery has been proven to improve fertility in women with minimal to mild disease and to reduce pain in women with mild to moderate endometriosis (5), justifying surgery in this population. It is important to emphasize that about 50% of subfertile women with endometriosis also had pain, and that cotreatment of both subfertility and pain is important in this group. The use of assisted reproductive technology (8) cannot be considered as a first-line infertility treatment of endometriosis (5). The possible risks of laparoscopic endometriosis surgery need to be acknowledged, but can be considered to be minimal when this surgery is done by experienced reproductive gynecological surgeons, in the context of a multidisciplinary center of excellence for endometriosis (9). Indeed, the integration of endometriosis care in such centers may be the only way to prevent overtreatment of women with endometriosis by assisted reproduction, potentially driven by the industrialization of assisted reproduction worldwide, and a useful way to embed endometriosis surgery in a larger context of reproductive medicine (9). Overall, the goal of infertility treatment in women with endometriosis should be to first surgically remove endometriosis and surgically treat associated pelvic pathology, and then to decide on expectant management, controlled ovarian stimulation with or without intrauterine insemination or assisted reproduction (8), based on female age, tubal condition after surgery, and duration of infertility. This strategy is currently evaluated in a prospective outcome study.

Christel Meuleman, M.D.a
Carla Tomassetti, M.D.a
Dirk Timmerman, M.D., Ph.D.b
Thomas D’Hooghe, M.D., Ph.D.a

a Leuven University Fertility Centre
Department of Obstetrics and Gynecology

b Department of Obstetrics and Gynecology
University Hospital Leuven

Leuven, Belgium

References
1. Meuleman C, Vandenabeele B, Fieuws S, Spiessens C, Timmerman D, D’Hooghe T
High prevalence of endometriosis in infertile women with normal ovulation and normospermic partners. Fertil Steril. 2009 Jul;92(1):68-74

2. National Collaboration Centre for Women’s and Childrens’ Health. Clinical Guideline 11: fertility: assessment and treatment for people with fertility problems. UK, NICE, 2004. http://www.nice.org.uk/nicemedia/pdf/CG011fullguideline.pdf

3. Bosteels J, Van Herendael B, Weyers S, D’Hooghe T. The position of diagnostic laparoscopy in current fertility practice Hum Reprod Update 2007; 13:477-85. Epub 2007 Jun 11.

4. Devlieger R, D’Hooghe T, Timmerman D. Uterine adenomyosis in the infertility clinic. Hum Reprod Update. 2003 Mar-Apr;9(2):139-47.

5. Kennedy S, Bergqvist A,Chapron C, D’Hooghe T, Dunselman G, Greb R, Hummelshoj L, Prentice A, Saridogan E. On behalf of the ESHRE Special Interest Group for Endometriosis and Endometrium Guideline Development Group.(the manuscript was prepared by the first author; all other authors contributed equally and are listed in alphabetical order) ESHRE Guideline for the Diagnosis and Treatment of Endometriosis. Hum Reprod 2005;20:2698-704.

6. Bazot M, Cortez A, Darai E, Rouger J, Chopier J, Antoine JM, Uzan S. Ultrasonography compared with magnetic resonance imaging for the diagnosis of adenomyosis: correlation with histopathology. Hum Reprod. 2001 Nov;16(11):2427-33.

7. Chapron Ch , Pietin-Vialle C , Borghese B, Davy C, Foulot H, Chopin N. Associated ovarian endometrioma is a marker for greater severity of deeply infiltrating endometriosis. Fertil Steril 2009 Aug ; 92 (2) : 453-7.

8. Zegers-Hochschild F, Adamson GD, de Mouzon J, Ishihara O, Mansour R, Nygren K, Sullivan E, and van der Poel S, on behalf of ICMART and WHO.The International Committee for Monitoring Assisted Reproductive Technology (ICMART) and the World Health Organization (WHO) Revised Glossary on ART Terminology, 2009.Hum Reprod 2009;24:2683-7.

9. D’Hooghe TM, Hummelshoj L. Multi-disciplinary centres/networks of excellence for endometriosis management and research: a proposal. Hum Reprod 2006;21(11):2743-8.

Published online in Fertility and Sterility doi:10.1016/j.fertnstert.2009.11.028

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