Sonographic Signs of Adenomyosis Are Prevalent in Women Undergoing Surgery for Endometriosis and May Suggest a Higher Risk of Infertility

Vered H Eisenberg, Nissim Arbib, Eyal Schiff, Motti Goldenberg, Daniel S Seidman, David Soriano, Vered H Eisenberg, Nissim Arbib, Eyal Schiff, Motti Goldenberg, Daniel S Seidman, David Soriano

Abstract

Objectives: To determine the prevalence of ultrasound features suggestive of adenomyosis in women undergoing surgery for endometriosis compared with a control group of healthy women without endometriosis.

Methods: Retrospective case-control study comparing women with intractable pain or infertility, who underwent transvaginal ultrasound and subsequent laparoscopic surgery, with a control group of healthy women without a previous history of endometriosis. A diagnosis of adenomyosis on TVUS was made based on asymmetrical myometrial thickening, linear striations, myometrial cysts, hyperechoic islands, irregular endometrial-myometrial junction, parallel shadowing, and localized adenomyomas and analyzed for one sign and for three or more signs.

Results: The study and control groups included 94 and 60 women, respectively. In the study group, women were younger and had more dysmenorrhea and infertility symptoms. The presence of any sonographic feature of adenomyosis, as well as three or more signs, was found to be more prevalent in the study group, which persisted after controlling for age, for all features but linear striations. Women in the study group who had five or more sonographic features of adenomyosis had more than a threefold risk of suffering from infertility (OR = 3.19, p = 0.015, 95% CI; 1.25-8.17). There was no association with disease severity at surgery.

Conclusions: Sonographic features of adenomyosis are more prevalent in women undergoing surgery for endometriosis compared to healthy controls. Women with more than five features had an increased risk of infertility.

Figures

Figure 1
Figure 1
Parallel shadowing. 2D image in transverse view of a uterus with parallel hypoechoic lines through the myometrium (arrow).
Figure 2
Figure 2
Asymmetrical myometrial thickening. 2D longitudinal view of a uterus with asymmetrical distances from the endometrium to the anterior and posterior serosal surfaces (arrows).
Figure 3
Figure 3
Severe adenomyosis with multiple sonographic signs: multiplanar and 3D rendering of an anteverted uterus with multiple sonographic signs: myometrial cysts (white arrow), hyperechoic islands (yellow arrow), linear striations (green arrow), and irregular EMJ (black arrow).
Figure 4
Figure 4
Localized adenomyoma. 2D image of an anteverted uterus with a localized adenomyoma in the posterior fundal wall (between yellow arrows).

References

    1. Vercellini P., Parazzini F., Oldani S., Panazza S., Bramante T., Crosignani P. G. Surgery: Adenomyosis at hysterectomy: a study on frequency distribution and patient characteristics. Human Reproduction. 1995;10(5):1160–1162. doi: 10.1093/oxfordjournals.humrep.a136111.
    1. Bergholt T., Eriksen L., Berendt N., Jacobsen M., Hertz J. B. Prevalence and risk factors of adenomyosis at hysterectomy. Human Reproduction. 2001;16(11):2418–2421. doi: 10.1093/humrep/16.11.2418.
    1. Reid P. C., Mukri F. Trends in number of hysterectomies performed in England for menorrhagia: examination of health episode statistics, 1989 to 2002-3. British Medical Journal. 2005;330(7497):938–939. doi: 10.1136/.
    1. Mehasseb M. K., Habiba M. A. Adenomyosis uteri: an update. The Obstetrician & Gynaecologist. 2009;11(1):41–47. doi: 10.1576/toag.11.1.41.27467.
    1. Struble J., Reid S., Bedaiwy M. A. Adenomyosis: a clinical review of a challenging gynecologic condition. Journal of Minimally Invasive Gynecology. 2016;23(2):164–185. doi: 10.1016/j.jmig.2015.09.018.
    1. 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. Human Reproduction. 2005;20(8):2309–2316. doi: 10.1093/humrep/dei021.
    1. Bazot M., Fiori O., Darai E. Adenomyosis in endometriosis—prevalence and impact on fertility. Evidence from magnetic resonance imaging. Human Reproduction. 2006;21(4):1101–1102. doi: 10.1093/humrep/dei448.
    1. Campo S., Campo V., Benagiano G. Adenomyosis and infertility. Reproductive BioMedicine Online. 2012;24(1):35–46. doi: 10.1016/j.rbmo.2011.10.003.
    1. Maheshwari A., Gurunath S., Fatima F., Bhattacharya S. Adenomyosis and subfertility: a systematic review of prevalence, diagnosis, treatment and fertility outcomes. Human Reproduction Update. 2012;18(4):374–392. doi: 10.1093/humupd/dms006.dms006
    1. Mathieu D'Argent E., Coutant C., Ballester M., et al. Results of first in vitro fertilization cycle in women with colorectal endometriosis compared with those with tubal or male factor infertility. Fertility and Sterility. 2010;94(6):2441–2443. doi: 10.1016/j.fertnstert.2010.03.033.
    1. Vercellini P., Consonni D., Barbara G., Buggio L., Frattaruolo M. P., Somigliana E. Adenomyosis and reproductive performance after surgery for rectovaginal and colorectal endometriosis: a systematic review and meta-analysis. Reproductive BioMedicine Online. 2014;28(6):704–713. doi: 10.1016/j.rbmo.2014.02.006.
    1. Dueholm M. Transvaginal ultrasound for diagnosis of adenomyosis: a review. Best Practice and Research: Clinical Obstetrics and Gynaecology. 2006;20(4):569–582. doi: 10.1016/j.bpobgyn.2006.01.005.
    1. Kepkep K., Tuncay Y. A., Göynümer G., Tutal E. Transvaginal sonography in the diagnosis of adenomyosis: which findings are most accurate? Ultrasound in Obstetrics and Gynecology. 2007;30(3):341–345. doi: 10.1002/uog.3985.
    1. 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. Human Reproduction. 2012;27(12):3432–3439. doi: 10.1093/humrep/des332.
    1. Dueholm M., Lundorf E., Hansen E. S., Sorensen J. S., Ledertoug S., Olesen F. Magnetic resonance imaging and transvaginal ultrasonography for the diagnosis of adenomyosis. Fertility and Sterility. 2001;76(3):588–594. doi: 10.1016/S0015-0282(01)01962-8.
    1. Bazot M., Cortez A., Darai E., et al. Ultrasonography compared with magnetic resonance imaging for the diagnosis of adenomyosis: correlation with histopathology. Human Reproduction. 2001;16(11):2427–2433. doi: 10.1093/humrep/16.11.2427.
    1. Reinhold C., McCarthy S., Bret P. M., et al. Diffuse adenomyosis: comparison of endovaginal US and MR imaging with histopathologic correlation. Radiology. 1996;199(1):151–158. doi: 10.1148/radiology.199.1.8633139.
    1. Meredith S. M., Sanchez-Ramos L., Kaunitz A. M. Diagnostic accuracy of transvaginal sonography for the diagnosis of adenomyosis: systematic review and metaanalysis. American Journal of Obstetrics and Gynecology. 2009;201(1):107e1–107e6. doi: 10.1016/j.ajog.2009.03.021.
    1. Abrao M. S., da C Gonçalves M. O., Dias J. A., Jr., Podgaec S., Chamie L. P., Blasbalg R. Comparison between clinical examination, transvaginal sonography and magnetic resonance imaging for the diagnosis of deep endometriosis. Human Reproduction. 2007;22(12):3092–3097. doi: 10.1093/humrep/dem187.
    1. Bazot M., Lafont C., Rouzier R., Roseau G., Thomassin-Naggara I., Daraï E. Diagnostic accuracy of physical examination, transvaginal sonography, rectal endoscopic sonography, and magnetic resonance imaging to diagnose deep infiltrating endometriosis. Fertility and Sterility. 2009;92(6):1825–1833. doi: 10.1016/j.fertnstert.2008.09.005.
    1. Hudelist G., Ballard K., English J., et al. Transvaginal sonography vs. clinical examination in the preoperative diagnosis of deep infiltrating endometriosis. Ultrasound in Obstetrics and Gynecology. 2011;37(4):480–487. doi: 10.1002/uog.8935.
    1. Lazzeri L., Di Giovanni A., Exacoustos C., et al. Preoperative and postoperative clinical and transvaginal ultrasound findings of adenomyosis in patients with deep infiltrating endometriosis. Reproductive Sciences. 2014;21(8):1027–1033. doi: 10.1177/1933719114522520.
    1. Levy G., Dehaene A., Laurent N., et al. An update on adenomyosis. Diagnostic and Interventional Imaging. 2013;94(1):3–25. doi: 10.1016/j.fertnstert.2009.03.012. doi: 10.1016/j.diii.2012.10.012.
    1. Bromley B., Shipp T. D., Benacerraf B. Adenomyosis: sonographic findings and diagnostic accuracy. Journal of Ultrasound in Medicine. 2000;19(8):529–534. doi: 10.7863/jum.2000.19.8.529.
    1. Reinhold C., Atri M., Mehio A., Zakarian R., Aldis A. E., Bret P. M. Diffuse uterine adenomyosis: morphologic criteria and diagnostic accuracy of endovaginal sonography. Radiology. 1995;197(3):609–614. doi: 10.1148/radiology.197.3.7480727.
    1. Exacoustos C., Brienza L., Di Giovanni A., et al. Adenomyosis: three-dimensional sonographic findings of the junctional zone and correlation with histology. Ultrasound in Obstetrics and Gynecology. 2011;37(4):471–479. doi: 10.1002/uog.8900.
    1. Exacoustos C., Manganaro L., Zupi E. Imaging for the evaluation of endometriosis and adenomyosis. Best Practice and Research: Clinical Obstetrics and Gynaecology. 2014;28(5):655–681. doi: 10.1016/j.bpobgyn.2014.04.010.
    1. Fedele L., Bianchi S., Dorta M., Zanotti F., Brioschi D., Carinelli S. Transvaginal ultrasonography in the differential diagnosis of adenomyoma versus leiomyoma. American Journal of Obstetrics and Gynecology. 1992;167(3):603–606. doi: 10.1016/S0002-9378(11)91558-0.
    1. Canis M., Donnez J. G., Guzick D. S., et al. Revised American Society for Reproductive Medicine classification of endometriosis: 1996. Fertility and Sterility. 1997;67(5):817–821. doi: 10.1016/S0015-0282(97)81391-X.
    1. Van Den Bosch T., Dueholm M., Leone F. P. G., et al. Terms, definitions and measurements to describe sonographic features of myometrium and uterine masses: a consensus opinion from the Morphological Uterus Sonographic Assessment (MUSA) group. Ultrasound in Obstetrics and Gynecology. 2015;46(3):284–298. doi: 10.1002/uog.14806.
    1. Brosens J., de Souza N. M., Barker F. G., Paraschos T., Winston R. M. L. Endovaginal ultrasonography in the diagnosis of adenomyosis uteri: identifying the predictive characteristics. BJOG: An International Journal of Obstetrics & Gynaecology. 1995;102(6):471–474. doi: 10.1111/j.1471-0528.1995.tb11320.x.
    1. Exacoustos C., Luciano D., Corbett B., et al. The uterine junctional zone: a 3-dimensional ultrasound study of patients with endometriosis. American Journal of Obstetrics and Gynecology. 2013;209(3):248.e1–248.e7. doi: 10.1016/j.ajog.2013.06.006.
    1. Kissler S., Zangos S., Wiegratz I., et al. Utero-tubal sperm transport and its impairment in endometriosis and adenomyosis. Annals of the New York Academy of Sciences. 2007;1101:38–48. doi: 10.1196/annals.1389.036.
    1. Vercellini P., Consonni D., Dridi D., Bracco B., Frattaruolo M. P., Somigliana E. Uterine adenomyosis and in vitro fertilization outcome: a systematic review and meta-analysis. Human Reproduction. 2014;29(5):964–977. doi: 10.1093/humrep/deu041.
    1. Galliano D., Bellver J., Díaz-García C., Simón C., Pellicer A. Art and uterine pathology: how relevant is the maternal side for implantation? Human Reproduction Update. 2015;21(1):13–38. doi: 10.1093/humupd/dmu047.dmu047

Source: PubMed

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