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Reproductive Biology and Endocrinology
Published in: Reproductive Biology and Endocrinology 1/2016

Open Access 01-12-2016 | Research

Adenomyosis in infertile women: prevalence and the role of 3D ultrasound as a marker of severity of the disease

Authors: J. M. Puente, A. Fabris, J. Patel, A. Patel, M. Cerrillo, A. Requena, J. A. Garcia-Velasco

Published in: Reproductive Biology and Endocrinology | Issue 1/2016

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Abstract

Background

Adenomyosis is linked to infertility, but the mechanisms behind this relationship are not clearly established. Similarly, the impact of adenomyosis on ART outcome is not fully understood. Our main objective was to use ultrasound imaging to investigate adenomyosis prevalence and severity in a population of infertile women, as well as specifically among women experiencing recurrent miscarriages (RM) or repeated implantation failure (RIF) in ART.

Methods

Cross-sectional study conducted in 1015 patients undergoing ART from January 2009 to December 2013 and referred for 3D ultrasound to complete study prior to initiating an ART cycle, or after ≥3 IVF failures or ≥2 miscarriages at diagnostic imaging unit at university-affiliated private IVF unit. Adenomyosis was diagnosed in presence of globular uterine configuration, myometrial anterior-posterior asymmetry, heterogeneous myometrial echotexture, poor definition of the endometrial-myometrial interface (junction zone) or subendometrial cysts. Shape of endometrial cavity was classified in three categories: 1.-normal (triangular morphology); 2.- moderate distortion of the triangular aspect and 3.- “pseudo T-shaped” morphology.

Results

The prevalence of adenomyosis was 24.4 % (n = 248) [29.7 % (94/316) in women aged ≥40 y.o and 22 % (154/699) in women aged <40 y.o., p = 0.003)]. Its prevalence was higher in those cases of recurrent pregnancy loss [38.2 % (26/68) vs 22.3 % (172/769), p < 0.005] and previous ART failure [34.7 % (107/308) vs 24.4 % (248/1015), p < 0.0001]. The presence of adenomyosis has been shown to be associated to endometriosis [35.1 % (34/97)]. Adenomyosis was diagnosed as a primary finding “de novo” in 80.6 % (n = 200) of the infertile patients. The impact on the uterine cavity was mild, moderate and severe in 63.7, 22.6 and 10.1 % of the cases, respectively.

Conclusions

Our results indicate that adenomyosis is a clinical condition with a high prevalence that may affect the reproductive results. The described severity criteria may help future validating studies for better counseling of infertile couples.
Literature
1.
Bird CC, McElin TW, Manalo-Estrella P. The elusive adenomyosis of the uterus--revisited. Am J Obstet Gynecol. 1972;112:583–93.CrossRefPubMed
2.
3.
Naftalin J, Hoo W, Nunes N, Mavrelos D, Nicks H, Jurkovic D. Inter and intra-observer variability in 3D ultrasound assessment of the endometrial-myometrial JZ and factors affecting its visualisation. Ultrasound Obstet Gynecol. 2012;39:587–91.CrossRefPubMed
4.
5.
Ballester M, d’Argent EM, Morcel K, Belaisch-Allart J, Nisolle M, Daraï E. Cumulative pregnancy rate after ICSI-IVF in patients with colorectal endometriosis: results of a multicentre study. Hum Reprod. 2012;27:1043–9.CrossRefPubMed
6.
Maubon A, Faury A, Kapella M, Pouquet M, Piver P. Uterine JZal zone at magnetic resonance imaging: a predictor of in vitro fertilization implantation failure. J Obstet Gynaecol Res. 2010;36:611–8.CrossRefPubMed
7.
Thalluri V, Tremellen KP. Ultrasound diagnosed adenomyosis has a negative impact on successful implantation following GnRH antagonist IVF treatment. Hum Reprod. 2012;27:3487–92.CrossRefPubMed
8.
Youm HS, Choi YS, Han HD. In vitro fertilization and embryo transfer outcomes in relation to myometrial thickness. J Assist Reprod Genet. 2011;28:1135–40.CrossRefPubMedPubMedCentral
9.
Benaglia L, Cardellicchio L, Leonardi M, Faulisi S, Vercellini P, Paffoni A, Somigliana E, Fedele L. Asymptomatic adenomyosis and embryo implantation in IVF cycles. Reprod Biomed Online. 2014;29(5):606–11.CrossRefPubMed
10.
Costello MF, Lindsay K, McNally G. The effect of adenomyosis on in vitro fertilisation and intra-cytoplasmic sperm injection treatment outcome. Eur J Obstet Gynecol Reprod Biol. 2011;158:229–34.CrossRefPubMed
11.
Martínez-Conejero JA, Morgan M, Montesinos M, Fortuño S, Meseguer M, Simón C, Horcajadas JA, Pellicer A. Adenomyosis does not affect implantation, but is associated with miscarriage in patients undergoing oocyte donation. Fertil Steril. 2011;96:943–50.CrossRefPubMed
12.
Mijatovic V, Florijn E, Halim N, Schats R, Hompes P. Adenomyosis has no adverse effects on IVF/ICSI outcomes in women with endometriosis treated with long-term pituitary down-regulation before IVF/ICSI. Eur J Obstet Gynecol Reprod Biol. 2010;151:62–6.CrossRefPubMed
13.
Mochimaru A, Aoki S, Oba MS, Kurasawa K, Takahashi T, Hirahara F. Adverse pregnancy outcomes associated with adenomyosis with uterine enlargement. J Obstet Gynaecol Res. 2014;3:1–5.
14.
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;20:2309–16.CrossRefPubMed
15.
Garcia L, Isaacson K. Adenomyosis: review of the literature. J Minim Invasive Gynecol. 2011;73:428–37.CrossRef
16.
Vercellini P, Vigano P, Somigliana E, Daguati R, Abbiati A, Fedele L. Adenomyosis: epidemiological factors. Best Pract Res Clin Obstet Gynaecol. 2006;20:465–77.CrossRefPubMed
17.
Mehasseb M, Habiba M. Adenomyosis uteri: an update. Obstet Gynecol. 2009;11:41–7.CrossRef
18.
Gordts S, Brosens JJ, Fusi L, Benagiano G, Brosens I. Uterine adenomyosis: a need for uniform terminology and consensus classification. Reprod Biomed Online. 2008;17:244–8.CrossRefPubMed
19.
ASRM Practice Committee. Definitions of infertility and recurrent pregnancy loss: a committee opinion. Fertil Steril. 2013;99:63.CrossRef
20.
Brosens JJ, Barker FG, de Souza NM. Myometrial zonal differentiation and uterine JZ zone hyperplasia in the non-pregnant uterus. Hum Reprod Update. 1998;4:496–502.CrossRefPubMed
21.
Asher SM, Arnold LL, Patt RH, Schruefer JJ, Bagley AS, Semelka RC, Zeman RK, Simon JA. Adenomyosis: prospective comparison of MR imaging and transvaginal sonography. Radiology. 1994;190:803–6.CrossRef
22.
Brosens JJ, De Souza NM, Barker FG, Paraschos T, Winston RM. Endovaginal ultrasonography in the diagnosis of adenomyosis uteri: Identifying the predictive characteristics. Br J Obstet Gynaecol. 1995;102:471–4.CrossRefPubMed
23.
Hirai M, Shibata K, Sagai H, Sekiya S, Goldberg BB. Transvaginal pulsed and color Doppler sonography for the evaluation of adenomyosis. J Ultrasound Med. 1995;14:529–32.PubMed
24.
Fedele L, Bianchi S, Dorta M, Arcaini L, Zanotti F, Carinelli S. Transvaginal ultrasonography in the diagnosis of diffuse adenomyosis. Fertil Steril. 1992;58:94–7.CrossRefPubMed
25.
Atri M, Reinhold C, Mehio AR, Chapman WB, Bret PM. Adenomyosis: US features with histologic correlation in an in-vitro study. Radiology. 2000;215:783–90.CrossRefPubMed
26.
Reinhold C, Atri M, Mehio A, Zakarian R, Aldis AE, Bret PM. Diffuse uterine adenomyosis: morphologic criteria and diagnostic accuracy of endovaginal sonography. Radiology. 1995;197:609–14.CrossRefPubMed
27.
Dueholm M. Transvaginal ultrasound for diagnosis of adenomyosis: a review. Best Pract Res Clin Obstet Gynaecol. 2006;20:569–82.CrossRefPubMed
28.
Devlieger R, D’Hooghe T, Timmerman D. Uterine adenomyosis in the infertility clinic. Hum Reprod Update. 2003;9:139–47.CrossRefPubMed
29.
Exacoustos C, Luciano D, Corbett B, De Felice G, Di Feliciantonio M, Luciano A, Zupi E. The uterine JZal zone: a 3-dimensional ultrasound study of patients with endometriosis. Am J Obstet Gynecol. 2013;209:248.e1–7.CrossRefPubMed
30.
Steer CV, Campbell S, Tan SL, Crayford T, Mills C, Mason BA, Collins WP. The use of transvaginal color flow imaging after in vitro fertilization to identify optimum uterine conditions before embryo transfer. Fertil Steril. 1992;57:372–6.CrossRefPubMed
31.
Timmerman D, Valentin L, Bourne TH, Collins WP, Verrelst H, Vergote I, International Ovarian Tumor Analysis (IOTA) Group. Terms, definitions and measurements to describe the sonographic features of adnexal tumors: a consensus opinion from the International Ovarian Tumor Analysis (IOTA) Group. Ultrasound Obstet Gynecol. 2000;16:500–5.CrossRefPubMed
32.
Ameye L, Timmerman D, Valentin L, Paladini D, Zhang J, Van Holsbeke C, Lissoni AA, Savelli L, Veldman J, Testa AC, Amant F, Van Huffel S, Bourne T. Clinically oriented three-step strategy for assessment of adnexal pathology. Ultrasound Obstet Gynecol. 2012;40:582–91.CrossRefPubMed
33.
Hudelist G, Fritzer N, Staettner S, Tammaa A, Tinelli A, Sparic R, Keckstein J. Uterine sliding sign: a simple sonographic predictor for presence of deep infiltrating endometriosis of the rectum. Ultrasound Obstet Gynecol. 2013;41(6):692–5.CrossRefPubMed
34.
Abrão MS, Gonçalves MO, Ajossa S, Melis GB, Guerriero S. The sonographic diagnosis of deep endometriosis. J Ultrasound Med. 2009;28:408–9.PubMed
35.
Guerriero S, Saba L, Ajossa S, Peddes C, Angiolucci M, Perniciano M, Melis GB, Alcázar JL. Three-dimensional ultrasonography in the diagnosis of deep endometriosis. Hum Reprod. 2014;29:1189–98.CrossRefPubMed
36.
Guerriero S, Ajossa S, Gerada M, Virgilio B, Angioni S, Melis GB. Diagnostic value of transvaginal “tenderness-guided” ultrasonography for the prediction of location of deep endometriosis. Hum Reprod. 2008;23:2452–7.CrossRefPubMed
37.
Meredith SM, Sanchez-Ramos L, Kaunitz AM. Diagnostic accuracy of transvaginal sonography for the diagnosis of adenomyosis: systematic review and meta-analysis. Am J Obstet Gynecol. 2009;201:107–12.CrossRefPubMed
38.
Maheshwari A. Adenomyosis and subfertility: a systematic review of prevalence, diagnosis, treatment and fertility outcomes. Hum Reprod Update. 2012;18:374–92.CrossRefPubMed
39.
Luciano DE, Exacoustos C, Albrecht L, LaMonica R, Proffer A, Zupi E, Luciano AA. Three-dimensional ultrasound in diagnosis of adenomyosis: histologic correlation with ultrasound targeted biopsies of the uterus. J Minim Invasive Gynecol. 2013;20:803–10.CrossRefPubMed
40.
Genc M, Genc B, Cengiz H. Adenomyosis and accompanying gynaecological pathologies. Arch Gynecol Obstet. 2014;4:877–81.
41.
Reid S, Lu C, Casikar I, Reid G, Abbott J, Cario G, Chou D, Kowalski D, Cooper M, Condous G. Prediction of pouch of Douglas obliteration in women with suspected endometriosis using a new real-time dynamic transvaginal ultrasound technique: the sliding sign. Ultrasound Obstet Gynecol. 2013;41:685–91.CrossRefPubMed
42.
Dueholm M, Lundorf E. Transvaginal ultrasound or MRI for diagnosis of adenomyosis. Curr Opin Obstet Gynecol. 2007;19:505–12.CrossRefPubMed
43.
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;16:2427–33.PubMed
44.
Reinhold C, Tafazoli F, Mehio A, et al. Uterine adenomyosis: endovaginal US and MR imaging features with histopathologic correlation. Radiographics. 1999;19(Spec No):S147–60.CrossRefPubMed
45.
Champaneria R, Abedin P, Daniels J, Balogun M, Khan KS. Ultrasound scan and magnetic resonance imaging for the diagnosis of adenomyosis: systematic review comparing test accuracy. Acta Obstet Gynecol Scand. 2010;89:1374–84.CrossRefPubMed
46.
Vercellini P, Consonni D, Dridi D, Bracco B, Frattaruolo MP, Somigliana E. Uterine adenomyosis and in vitro fertilization outcome: a systematic review and meta-analysis. Hum Reprod. 2014;29:964–77.CrossRefPubMed
47.
Di Donato N, Seracchioli R. How to evaluate adenomyosis in patients affected by endometriosis? Minim Invasive Surg. 2014.
48.
Yeniel O, Cirpan T, Ulukus M, Ozbal A, Gundem G, Ozsener S, Zekioglu O, Yilmaz H. Adenomyosis: prevalence, risk factors, symptoms and clinical findings. Clin Exp Obstet Gynecol. 2007;34:163–7.PubMed
49.
Gianaroli L, Racowsky C, Geraedts J, Cedars M, Makrigiannakis A, Lobo R. Best practices of ASRM and ESHRE: a journey through reproductive medicine. Hum Reprod. 2012;27:3365–79.CrossRefPubMed
50.
Taran FA, Stewart EA, Brucker S. Adenomyosis: epidemiology, risk factors, clinical phenotype and surgical and interventional alternatives to hysterectomy. Geburtshilfe Frauenheilkd. 2013;73:924–31.CrossRefPubMedPubMedCentral
51.
Leyendecker G, Bilgicyildirim A, Inacker M, Stalf T, Huppert P, Mall G, Böttcher B, Wildt L. Adenomyosis and endometriosis. Re-visiting their association and further insights into the mechanisms of auto-traumatisation. An MRI study. Arch Gynecol Obstet. 2015;291:917–32.CrossRefPubMed
52.
Brosens I, Pijnenborg R, Benagiano G. Defective myometrial spiral artery remodelling as a cause of major obstetrical syndromes in endometriosis andadenomyosis. Placenta. 2013;34:100–5.CrossRefPubMed
53.
Salim R, Riris S, Saab W, Abramov B, Khadum I, Serhal P. Adenomyosis reduces pregnancy rates in infertile women undergoing IVF. Reprod Biomed Online. 2012;25:273–7.CrossRefPubMed
54.
Struble J, Reid S, Bedaiwy MA. Adenomyosis: a clinical review of a challenging gynecologic condition. J Minim Invasive Gynecol. 2016;23(2):164–85.CrossRefPubMed
55.
Galliano D, Bellver J, Díaz-García C, Simón C, Pellicer A. ART and uterine pathology: how relevant is the maternal side for implantation. Hum Reprod Update. 2015;21:13–38.CrossRefPubMed
Metadata
Title
Adenomyosis in infertile women: prevalence and the role of 3D ultrasound as a marker of severity of the disease
Authors
J. M. Puente
A. Fabris
J. Patel
A. Patel
M. Cerrillo
A. Requena
J. A. Garcia-Velasco
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2016
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/s12958-016-0185-6

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