The role of cine MR imaging in the assessment of uterine function

Purpose To review the literature on uterine contraction and to highlight magnetic resonance imaging using the cine technique as a useful method to evaluate these movements.

The literature research on PubMed database was done up to February 2019 with restriction to English language about articles regarding uterine peristalsis and cine MR.

Infertility is a common clinical problem and a source of frustration for those who want to have children. Uterine movements are crucial elements in respect of successful conception, implantation, and the development of a healthy pregnancy. It is known that the direction and frequency of uterine peristalsis are closely related to the different phases of the menstrual cycle, and that changes in its activity may interfere with reproduction. One condition that has been linked with infertility by several studies is dysfunctional uterine contractility. Magnetic resonance imaging, using the cine technique, has been shown to be a useful tool in the evaluation of these movements, allowing the identification of patients with some type of dysfunction and establish strategies to increase pregnancy rates.

Cine MR is an excellent imaging method for the evaluation of uterine peristalsis and identification of dysfunctional contractions. Similar content being viewed by others

Giudice LC (2010) Clinical practice: endometriosis. N Engl J Med 362(25):238998 Olive DL, Pritts EA (2001) Treatment of endometriosis. N Engl J Med 345:266–275 Abrao MS, Dias JA Jr, Bellelis P, Podgaec S, Bautzer CR, Gromatsky C (2009) Endometriosis of the ureter and bladder are not associated diseases. Fertil Steril. 91(5):1662–1667 Vigano P, Parazzini F, Somigliana E, Vercellini P (2004) Endometriosis: epidemiology and aetiological factors. Best Pract Res Clin Obstet Gynaecol 18:177–200 Sillou S, Poirée S, Millischer AE, Chapron C, Hélénon O (2015) Urinary endometriosis: MR imaging appearance with surgical and histological correlations. Diagn Interv Imaging. 96(4):373–381 Koninckx PR, Meuleman C, Demeyere S, Lesaffre E, Cornillie FJ (1991) Suggestive evidence that pelvic endometriosis is a progressive disease, whereas deeply infiltrating endometriosis is associated with pelvic pain. Fertil Steril 55(4):759–765 Williams TJ, Pratt JH (1977) Endometriosis in 1000 consecutive celiotomies: incidence and management. Am J Obstet Gynecol. 129(3):245–250 Ashrafi M, Sadatmahalleh SJ, Akhoond MR, Talebi M (2016) Evaluation of risk factors associated with endometriosis in infertile women. Int J Fertil Steril. 10(1):11–21 Kvaskoff M, Mu F, Terry KL et al (2015) Endometriosis: a high-risk population for 337 major chronic diseases? Hum Reprod Update 21:500–516 Parazzini F, Esposito G, Tozzi L, Noli S, Bianchi S (2017) Epidemiology of endometriosis and its comorbidities. Eur J Obstet Gynecol Reprod Biol. 209:3–7 Sinaii N, Cleary SD, Ballweg ML, Nieman LK, Stratton P (2002) High rates of autoimmune and endocrine disorders, fibromyalgia, chronic fatigue syndrome and atopic diseases among women with endometriosis: a survey analysis. Hum Reprod. 17(10):2715–2724 Kido A, Togashi K, Nishino M, Miyake K, Koyama T, Fujimoto R, Iwasaku K, Fujii S, Hayakawa K (2007) Cine MR imaging of uterine peristalsis in patients with endometriosis. Eur Radiol. 17(7):1813–1819 Matalliotakis IM, Goumenou AG, Matalliotakis M, Arici A (2010) Uterine anomalies in women with endometriosis. J Endometr. 2:213–217 Harada T, Khine YM, Kaponis A, Nikellis T, Decavalas G, Taniguchi F (2016) The impact of adenomyosis on women's fertility. Obstet Gynecol Surv. 71(9):557–568 Kunz G, Beil D, Huppert P, Noe M, Kissler S, Leyendecker G (2005) Adenomyosis in endometriosis-prevalence and impact on fertility: Evidence from magnetic resonance imaging. Hum Reprod. 20(8):2309–2316 Leyendecker G, Kunz G, Herbertz M, Beil D, Huppert P, Mall G, Kissler S, Noe M, Wildt L (2004) Uterine peristaltic activity and the development of endometriosis. Ann NY Acad Sci 1034:338–355 Noe M, Kunz G, Herbertz M, Mall G, Leyendecker G (1999) The cyclic pattern of the immunocytochemical expression of oestrogen and progesterone receptors in human myometrial and endometrial layers: characterisation of the endometrial-subendometrial unit. Hum Reprod 14:101–110 Togashi K (2007) Uterine contractility evaluated on cine magnetic resonance imaging. Ann NY Acad Sci. 1101:62–71 Hricak H, Alpers C, Crooks LE, Sheldon PE (1983) Magnetic resonance imaging of the female pelvis: initial experience. AJR Am J Roentgenol 141:1119–1128 Daido S, Kido A, Kataoka M, Nakai A, Fujimoto K, Kusahara H, Okada T, Togashi K (2017) MR imaging of uterine morphology and dynamic changes during lactation. J Magn Reson Imaging. 45(2):617–623 Togashi K, Nakai A, Sugimura K (2001) Anatomy and physiology of the female pelvis: MR imaging revisited. J Magn Reson Imaging 13(842):849 Bazot M, Bharwani N, Huchon C, Kinkel K, Cunha TM, Guerra A, Manganaro L, Buñesch L, Kido A, Togashi K, Thomassin-Naggara I, Rockall AG (2017) European society of urogenital radiology (ESUR) guidelines: MR imaging of pelvic endometriosis. Eur Radiol. 27(7):2765–2775 Lyons EA, Taylor PJ, Zheng XH, Ballard G, Levi CS, Kredentser JV (1991) Characterization of subendometrial myometrial contractions throughout the menstrual cycle in normal fertile women. Fertil Steril 55(4):771–774 Chalubinski K, Deutinger J, Bernaschek G (1993) Vaginosonography for recording of cycle-related myometrial contractions. Fertil Steril 59(1):225–228 Nakai A, Togashi K, Yamaoka T, Fujiwara T, Ueda H, Koyama T, Kobayashi H, Kagimura T, Fujii S, Konishi J (2003) Uterine peristalsis shown on cine MR imaging using ultrafast sequence. J Magn Reson Imaging 18:726–733 Liu S, Zhang Q, Yin C, Chen W, Chan Q, He J, Zhu B (2018) An optimised repetition time (TR) for cine imaging of uterine peristalsis on 3 T MRI. Clin Radiol. 73(7):678.e7–678.e12 Liu S, Zhang Q, Yin C, Liu S, Chan Q, Chen W, He J, Zhu B (2016) Optimized approach to cine MRI of uterine peristalsis. J Magn Reson Imaging. 44(6):1397–1404 Bazot M, Bornier C, Dubernard G, Roseau G, Cortez A, Darai E (2007) Accuracy of magnetic resonance imaging and rectal endoscopic sonography for the prediction of location of deep pelvic endometriosis. Hum Reprod 22:1457–1463 Brandão A, Crispi C, Pinho M (2014) Magnetic Resonance Atlas of Deep Endometriosis: MRI and Laparoscopic Correlations, 1st edn. Revinter, Rio de Janeiro Chamie LP, Blasbalg R, Goncalves MO, Carvalho FM, Abrao MS, de Oliveira IS (2009) Accuracy of magnetic resonance imaging for diagnosis and preoperative assessment of deep infiltrating endometriosis. Int J Gynaecol Obstet 106:198–201 Vimercati et al (2012) Accuracy of transvaginal sonography and contrast-enhanced magnetic resonance-colonography for the presurgical staging of deep infiltrating endometriosis. Ultrasound Obstet Gynecol 40(5):592–603 Marcal L, Nothaft MA, Coelho F, Volpato R, Iyer R (2011) Mullerian duct anomalies: MR imaging. Abdom Imaging. 36(6):756–764 Takeuchi M, Matsuzaki K (2011) Adenomyosis: usual and unusual imaging manifestations, pitfalls, and problem-solving MR imaging techniques. Radiographics. 31(1):99–115 Hottat N, Larrousse C, Anaf V et al (2009) Endometriosis: contribution of 30-T pelvic MR imaging in preoperative assessment—initial results. Radiology 253(1):126–134 Manganaro L, Fierro F, Tomei A et al (2012) Feasibility of 30-T pelvic MR imaging in the evaluation of endometriosis. Eur J Radiol 81(6):1381–1387 Rousset P, Peyron N, Charlot M et al (2014) Bowel endometriosis: preoperative diagnostic accuracy of 30-T MR enterography–initial results. Radiology 273(1):117–124 Steensma AB, van Santbrink EJ et al (2014) Can magnetic resonance imaging at 30-Tesla reliably detect patients with endometriosis? Initial results. J Obstet Gynaecol Res 40(4):1051–1058 Togashi K (1993) MR imaging of the female pelvis. Igaku-shoin, New York Fujiwara T et al (2004) Kinematics of the uterus: cine mode MR imaging. Radiographics 24:e19 Kido A, Ascher SM, Hahn W, Kishimoto K, Kashitani N, Jha RC, Togashi K, Spies JB (2014) 3 T MRI uterine peristalsis: comparison of symptomatic fibroid patients versus controls. Clin Radiol. 69(5):468–472 Leyendecker G, Kunz G, Noe M, Herbertz M, Mall G (1998) Endometriosis: a dysfunction and disease of the archimetra. Hum Reprod Update 4:752–762 Ijland MM, Evers JL, Dunselman GA, van Katwijk C, Lo CR, Hoogland HJ (1996) Endometrial wavelike movements during the menstrual cycle. Fertil. Steril. 65:746–749 Kuijsters NPM, Methorst WG, Kortenhorst MSQ, Rabotti C, Mischi M, Schoot BC (2017) Uterine peristalsis and fertility: current knowledge and future perspectives: a review and meta-analysis. Reprod Biomed Online. 35(1):50–71 Fanchin R, Righini C, Olivennes F, Taylor S, de Ziegler D, Frydman R (1998) Uterine contractions at the time of embryo transfer alter pregnancy rates after in- fertilization. Hum. Reprod. 13:1968–1974 Bellver J, Simón C (2018) Implantation failure of endometrial origin: what is new? Curr Opin Obstet Gynecol. 30(4):229–236 Kava-Braverman A, Martinez F, Rodriguez I et al (2017) What is a difficult transfer? Analysis of 7714 embryo transfers: the impact of maneuvers during embryo transfers on pregnancy rate and a proposal of objective assessment. Fertil Steril 107:657–663 Fanchin R, Ayoubi JM, Righini C, Olivennes F, Schonauer LM, Frydman R (2001) Uterine contractility decreases at the time of blastocyst transfers. Hum. Reprod. 16:1115–1119 Fanchin R, Righini C, de Ziegler D, Olivennes F, Ledee N, Frydman R (2001) Effects of vaginal progesterone administration on uterine contractility at the time of embryo transfer. Fertil. Steril. 75:1136–1140 Ayoubi JM, Epiney M, Brioschi PA, Fanchin R, Chardonnens D, de Ziegler D (2003) Comparison of changes in uterine contraction frequency after ovulation in the menstrual cycle and in in vitro fertilization cycles. Fertil. Steril. 79:1101–1105 Zhu L, Che HS, Xiao L, Li YP (2014) Uterine peristalsis before embryo transfer affects the chance of clinical pregnancy in fresh and frozen-thawed embryo transfer cycles. Hum. Reprod. 29:1238–1243 Huang QY, Rong MH, Lan AH et al (2017) The impact of atosiban on pregnancy outcomes in women undergoing in vitro fertilization-embryo transfer: a meta- analysis. PLoS ONE 12:e0175501 Li J, Chen Y, Wang A, Zhang H (2017) A meta-analysis of atosiban supplementation among patients undergoing assisted reproduction. Arch Gynecol Obstet 296:623–634 Leyendecker G, Kunz G, Wildt L, Beil D, Deininger H (1996) Uterine hyperperistalsis and dysperistalsis as dysfunctions of the mechanism of rapid sperm transport in patients with endometriosis and infertility. Hum Reprod 11(7):1542–1551. Funding No funding was received for the preparation of this review. Author information Authors and Affiliations Contributions DMS data collection, manuscript writing. HWJ, LKB and FPPLL manuscript editing. MAPO project development, data collection, manuscript editing. Corresponding author Ethics declarations Conflict of interest The authors declare that they have no conflict of interest. Ethical approval This article does not contain any studies with human participants or animals performed by any of the authors. Additional information Publisher's Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Electronic supplementary material Below is the link to the electronic supplementary material. Rights and permissions About this article Cite this article Soares, D.M., Junior, H.W., Bittencourt, L.K. et al. The role of cine MR imaging in the assessment of uterine function. Arch Gynecol Obstet 300, 545–553 (2019). https://doi.org/10.1007/s00404-019-05222-9 Received: Accepted: Published: Version of record: Issue date: DOI: https://doi.org/10.1007/s00404-019-05222-9