Adenomyosis and Subfertility: Evidence of Association and Causation

Carla Tomassetti; Christel Meuleman; Dirk Timmerman; Thomas D'Hooghe

doi:10.1055/s-0032-1333475

Seminars in Reproductive Medicine, Table of Contents

Semin Reprod Med 2013; 31(02): 101-108
DOI: 10.1055/s-0032-1333475

Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Adenomyosis and Subfertility: Evidence of Association and Causation

Carla Tomassetti

¹Department Obstetrics and Gynecology/Leuven University Fertility Center

,

Christel Meuleman

¹Department Obstetrics and Gynecology/Leuven University Fertility Center

,

Dirk Timmerman

²Department Obstetrics and Gynecology, University Hospitals Leuven, Leuven, Belgium

,

Thomas D'Hooghe

¹Department Obstetrics and Gynecology/Leuven University Fertility Center

› Author Affiliations

Abstract

Due to the confounding or unknown presence of endometriosis in both cases and controls, it is difficult to test the hypothesis that adenomyosis causes infertility. Based on the limited available evidence, there is evidence to support a causal association between adenomyosis and subfertility: Adenomyosis is associated with lifelong infertility in baboons, is associated with impaired reproductive outcome after assistive reproductive technique, and a dose–effect relationship between the degree of adenomyosis and the degree of abnormal uterotubal contractility has been demonstrated. More and better designed studies are needed to assess the impact of adenomyosis on infertility in women with the laparoscopic-proven presence or absence of endometriosis.

Keywords

adenomyosis - infertility - causality

Full Text

References

References
1 Devlieger R, D'Hooghe T, Timmerman D. Uterine adenomyosis in the infertility clinic. Hum Reprod Update 2003; 9 (2) 139-147
2 Azziz R. Adenomyosis: current perspectives. Obstet Gynecol Clin North Am 1989; 16 (1) 221-235
3 Deciding whether your treatment has done harm. In: Sackett DL, Haynes RB, Guyatt GH, Tugwell P, , eds. Clinical Epidemiology. Philadelphia, PA: Lippincott, Williams & Wilkins; 1991: 283-302
4 Harm. In: Sackett DL, Straus SE, Richardson WS, Rosenberg W, Haynes RB, , eds. Evidence-Based Medicine. How to Practice and Teach EBM. Edinburgh, UK: Churchill Livingstone; 2000: 155-168
5 Statistics for the non-statistician. In: Trisha Greenhalgh , ed. How to Read a Paper? The Basics of Evidence Based Medicine. London, UK: BMJ Books; 2001: 87
6 Maheshwari A, Gurunath S, Fatima F, Bhattacharya S. Adenomyosis and subfertility: a systematic review of prevalence, diagnosis, treatment and fertility outcomes. Hum Reprod Update 2012; 18 (4) 374-392
7 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 (11) 1374-1384
8 Naftalin J, Hoo W, Pateman K, Mavrelos D, Holland T, Jurkovic D. How common is adenomyosis? A prospective study of prevalence using transvaginal ultrasound in a gynaecology clinic. Hum Reprod 2012; 27 (12) 3432-3439
9 Benagiano G, Habiba M, Brosens I. The pathophysiology of uterine adenomyosis: an update. Fertil Steril 2012; 98 (3) 572-579
10 D'Hooghe TM, Debrock S, Hill JA, Meuleman C. Endometriosis and subfertility: is the relationship resolved?. Semin Reprod Med 2003; 21 (2) 243-254
11 de Souza NM, Brosens JJ, Schwieso JE, Paraschos T, Winston RM. The potential value of magnetic resonance imaging in infertility. Clin Radiol 1995; 50 (2) 75-79
12 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 (8) 2309-2316
13 Kissler S, Zangos S, Kohl J , et al. Duration of dysmenorrhoea and extent of adenomyosis visualised by magnetic resonance imaging. Eur J Obstet Gynecol Reprod Biol 2008; 137 (2) 204-209
14 Kissler S, Hamscho N, Zangos S , et al. Uterotubal transport disorder in adenomyosis and endometriosis—a cause for infertility. BJOG 2006; 113 (8) 902-908
15 Bazot M, Fiori O, Darai E. Adenomyosis in endometriosis—prevalence and impact on fertility. Evidence from magnetic resonance imaging [comment]. Hum Reprod 2006; 21 (4) 1101-1102; author reply 1102–1103
16 Bazot M, Darai E, Hourani R , et al. Deep pelvic endometriosis: MR imaging for diagnosis and prediction of extension of disease. Radiology 2004; 232 (2) 379-389
17 Barrier BF, Malinowski MJ, Dick Jr EJ, Hubbard GB, Bates GW. Adenomyosis in the baboon is associated with primary infertility. Fertil Steril 2004; 82 (Suppl. 03) 1091-1094
18 Landi S, Mereu L, Pontrelli G , et al. The influence of adenomyosis in patients laparoscopically treated for deep endometriosis. J Minim Invasive Gynecol 2008; 15 (5) 566-570
19 Ferrero S, Anserini P, Abbamonte LH, Ragni N, Camerini G, Remorgida V. Fertility after bowel resection for endometriosis. Fertil Steril 2009; 92 (1) 41-46
20 Daraï E, Carbonnel M, Dubernard G , et al. Determinant factors of fertility outcomes after laparoscopic colorectal resection for endometriosis. Eur J Obstet Gynecol Reprod Biol 2010; 149 (2) 210-214
21 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 (4) 1043-1049
22 Kunz G, Beil D. Characterization of the uterine junctional zone prior to IVF/ICSI: an observational study. Arch Gynecol Obstet 2010; 281 (5) 945-953
23 Maubon A, Faury A, Kapella M, Pouquet M, Piver P. Uterine junctional zone at magnetic resonance imaging: a predictor of in vitro fertilization implantation failure. J Obstet Gynaecol Res 2010; 36 (3) 611-618
24 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 (1) 62-65
25 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 (2) 229-234
26 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 (3) 273-277
27 Tremellen K, Russell P. Adenomyosis is a potential cause of recurrent implantation failure during IVF treatment. Aust N Z J Obstet Gynaecol 2011; 51 (3) 280-283
28 Thalluri V, Tremellen KP. Ultrasound diagnosed adenomyosis has a negative impact on successful implantation following GnRH antagonist IVF treatment. Hum Reprod 2012; 27 (12) 3487-3492
29 Kennedy S, Bergqvist A, Chapron C , et al; ESHRE Special Interest Group for Endometriosis and Endometrium Guideline Development Group. ESHRE guideline for the diagnosis and treatment of endometriosis. Hum Reprod 2005; 20 (10) 2698-2704
30 Sallam HN, Garcia-Velasco JA, Dias S, Arici A. Long-term pituitary down-regulation before in vitro fertilization (IVF) for women with endometriosis. Cochrane Database Syst Rev 2006; 25 (1) CD004635
31 Martínez-Conejero JA, Morgan M, Montesinos M , et al. Adenomyosis does not affect implantation, but is associated with miscarriage in patients undergoing oocyte donation. Fertil Steril 2011; 96 (4) 943-950
32 Kissler S, Zangos S, Wiegratz I , et al. Utero-tubal sperm transport and its impairment in endometriosis and adenomyosis. Ann N Y Acad Sci 2007; 1101: 38-48
33 Campo S, Campo V, Benagiano G. Adenomyosis and infertility. Reprod Biomed Online 2012; 24 (1) 35-46
34 Leyendecker G, Kunz G, Kissler S, Wildt L. Adenomyosis and reproduction. Best Pract Res Clin Obstet Gynaecol 2006; 20 (4) 523-546
35 Kissler S, Hamscho N, Zangos S , et al. Diminished pregnancy rates in endometriosis due to impaired uterotubal transport assessed by hysterosalpingoscintigraphy. BJOG 2005; 112 (10) 1391-1396
36 Leyendecker G, Kunz G, Noe M, Herbertz M, Mall G. Endometriosis: a dysfunction and disease of the archimetra. Hum Reprod Update 1998; 4 (5) 752-762
37 Quinn M. Uterine innervation in adenomyosis. J Obstet Gynaecol 2007; 27 (3) 287-291
38 Kissler S, Wildt L, Schmiedehausen K , et al. Predictive value of impaired uterine transport function assessed by negative hysterosalpingoscintigraphy (HSSG). Eur J Obstet Gynecol Reprod Biol 2004; 113 (2) 204-208
39 Bromer JG, Aldad TS, Taylor HS. Defining the proliferative phase defect. Fertil Steril 2009; 91: 698-704
40 Ota H, Tanaka T. Stromal vascularization in the endometrium during adenomyosis. Microsc Res Tech 2003; 60 (4) 445-449
41 Fischer CP, Kayisili U, Taylor HS. HOXA10 expression is decreased in endometrium of women with adenomyosis. Fertil Steril 2011; 95 (3) 1133-1136
42 Xiao Y, Sun X, Yang X , et al. Leukemia inhibitory factor is dysregulated in the endometrium and uterine flushing fluid of patients with adenomyosis during implantation window. Fertil Steril 2010; 94 (1) 85-89
43 Yang JH, Wu MY, Chang DY, Chang CH, Yang YS, Ho HN. Increased interleukin-6 messenger RNA expression in macrophage-cocultured endometrial stromal cells in adenomyosis. Am J Reprod Immunol 2006; 55 (3) 181-187
44 Liu H, Lang J, Wang X, Wu S. Comparative proteomic analysis of human adenomyosis using two-dimensional gel electrophoresis and mass spectrometry. Fertil Steril 2008; 89 (6) 1625-1631
45 Grümmer R. Animal models in endometriosis research. Hum Reprod Update 2006; 12 (5) 641-649