Hardware visualization of adenomyosis and the reproductive outcomes of surgical treatment for adenomyosis-associated infertility

Krylov K.Yu., Rukhlyada N.N., Biryukova E.I., Tsechoeva L.Sh., Vinnikova S.V.

1) Saint Petersburg State Pediatric Medical University, Ministry of Health of Russia, Saint Petersburg, Russia; 2) I.I. Dzhanelidze Saint Petersburg Research Institute of Emergence Care, Saint Petersburg, Russia
The presented review includes an analysis of clinical trials evaluating the impact of adenomyosis on reproductive function, as well as a review of studies on the relationship between surgical treatment options for adenomyosis and reproductive outcomes. Studies of female populations after in vitro fertilization and/or intracytoplasmic sperm injection (IVF/ICSI) and after surgical treatment for deep adenomyosis have shown that adenomyosis has a negative impact on a reproductive outcome in both cases, although there are substantial differences in these populations. The literature contains relatively little data on the degree of influence of the extent of the lesion on reproductive function; however, a significant correlation has been found between them. The positive impact of treatment with gonadotropin-releasing hormone agonists, followed by surgery for adenomyosis, is also described in several sources of literature; however, no controlled trials have been conducted on this topic. Many studies do not meet the significance tests due to the lack of clear inclusion and exclusion criteria in the trial. It is difficult to choose optimal treatment options for adenomyosis based on actual data because there is no significant evidence for the relationship between fertility and the degree of adenomyosis. However, it is known that adenomyosis can reduce the chance of successful implantation so much that it will be reasonable to recommend surgical or other medical options. At the same time, it is necessary to evaluate the possible positive impact of the medical options available in the physician’s arsenal. Thus, timely referral to specialized healthcare facilities for the treatment of adenomyosis may be crucial for the successful implementation of reproductive function in patients with suspected or diagnosed adenomyosis concurrent with recurrent miscarriage, who refuse to use assisted reproductive technologies.
Conclusion. This review analyzes the relationship between infertility and adenomyosis and considers studies of reproductive outcomes after different surgical treatment options for adenomyosis in infertile patients.

Keywords

adenomyosis
infertility
assisted reproductive technologies
pregnancy
reproductive outcome
surgical treatment

References

  1. Адамян Л.В., Кулаков В.И., Андреева В.Н. Эндометриозы. М.: Медицина; 2006. 416с. [Adamyan L.V., Kulakov V.I., Andreeva V.N. Endometriosis. M.: Medicine, 2006. 416 p. (in Russian)].
  2. Бирюкова Е.И., Рухляда Н.Н., Крылов К.Ю. Аденомиоз: хирургический подход и репродуктивные исходы. Акушерство и гинекология. 2019; 5: 30-4. [Birukova E.I., Rukhliada N.N., Krylov K.Yu. Adenomyosis: Surgical Approach and Reproductive Outcomes. Obstetrics and gynecology. 2019; 5: 30-4. (in Russian)]. https://dx.doi.org/10.18565/aig.2019.5.30-34.
  3. Рухляда Н.Н., Крылов К.Ю., Бирюкова Е.И. Органосберегающие операции при аденомиозе. Акушерство и гинекология. 2019; 5: 86-9. [Rukhliada N.N., Krylov K.Yu., Birukova E.I. Organ-saving operations for adenomyosis. Obstetrics and gynecolo-gy. 2019; 5: 86-9 (in Russian)]. https://dx.doi.org/10.18565/aig.2019.5.86-89.
  4. Стрижаков А.Н., Давыдов А.И., Пашков В.М. Аденомиоз: возможности и перспективы эндохирургического лечения с учетом морфологического строения миометрия, эндометрия и яичников. Журнал акушерства и женских болезней. 2002; 51(3): 28-31. [Strizhakov A.N., Davydov A.I., Pashkov V.M. Adenomyosis: possibilities and prospects of endosurgical treatment taking into account the morphological structure of the myometrium, endometrium and ovaries. Journal of Obstetrics and Women's Diseases. 2002; 51(3): 28-31. (in Russian)].
  5. Радзинский В.Е., Гус А.И., Семятов С.М. и др. Эндометриоз: учебно-методическое пособие. М.: Изд-во РУДН; 2001. 64с. [Radzinsky V.E., Gus A.I., Semyatov S.M. et al. Endometriosis: teaching manual. M.; 2001. 64 p. (in Russian)].
  6. Rukhliada N.N., Krylov K.Y., Matukhin V.I. The quality of life of women and morphological changes in the glands of adenomyosis under the influence of dienogest-containing preparations. J. Endometr. Pelvic Pain Disorders. 2020; 12(3-4). https://dx.doi.org/10.1177/2284026520914143.
  7. Рухляда Н.Н., Крылов К.Ю., Бирюкова Е.И. Возможности органосберегающих операций при аденомиозе в аспекте сохранения репродуктивной функции. Акушерство и гинекология. 2018; 7: 120-4. [Rukhliada N.N., Krylov K.Y., Birukova E.I. Possibilities of organ-saving surgery for adenomyosis in terms of preserving reproductive function. Obstetrics and gynecology. 2018; 7: 120-4. (in Russian)]. https://dx.doi.org/10.18565/aig.2018.7.120-124.
  8. Exacoustos C., Brienza L., Di Giovanni A., Szabolcs B., Romanini M.E., Zupi E., Arduini D. Adenomyosis: three-dimensional sonographic findings of the junc-tional zone and correlation with histology. Ultrasound Obstet. Gynecol. 2011; 37(4): 471-9. https://dx.doi.org/10.1002/uog.8900.
  9. Рухляда Н.Н., Аракелян Б.В., Прохорович Т.И., Либова Т.А., Крылов К.Ю. Аденомиоз: современные подходы к хирургическому лечению. Учебно-методическое пособие. Серия: Библиотека педиатрического университета. СПб.; 2020. 16с. [Rukhliada N.N., Arakelyan B.V., Prohorovich T.I., Libova T.A., Krylov K.Yu. Adenomyosis: modern approaches to surgical treatment. Education-al-methodical handbook. Pediatric University Library. 2020. St. Petersburg. 16 p. (in Russian)].
  10. 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): 2309-16. https://dx.doi.org/10.1093/humrep/dei021.
  11. Champaneria R., Abedin P., Daniels J., Balogun M., Khan K.S. Ultrasound scan and magnetic resonance imaging for the diagnosis of adenomyosis: systematic review comparing test accuracy. Acta Obstet. Gynecol. Scand. 2010; 89(11): 1374-84. https://dx.doi.org/10.3109/00016349.2010.512061.
  12. Rukhliada N.N., Krylov K.Y. Adenomyosis and adenomyomectomy experience. Global Reprod. 2019; 2: 5-12.
  13. Gordts S., Brosens J.J., Fusi L., Benagiano G., Brosens I. Uterine adenomyo-sis: a need for uniform terminology and consensus classification. Reprod. Biomed. Online. 2008; 17(2): 244-8. https://dx.doi.org/10.1016/s1472-6483(10)60201-5.
  14. Puente J.M., Fabris A., Patel J., Patel A., Cerrillo M., Requena A. et al. Ade-nomyosis in infertile women: prevalence and the role of 3D ultrasound as a marker of severity of the disease. Reprod. Biol. Endocrinol. 2016; 14(1): 60. https://dx.doi.org/10.1186/s12958-016-0185-6.
  15. Lazzarin N., Exacoustos C., Vaquero E., De F.G., Manfellotto D., Zupi E. Uterine junctional zone at three-dimensional transvaginal ultrasonography in patients with recurrent miscarriage: a new diagnostic tool? Eur. J. Obstet. Gynecol. Reprod. Biol. 2014; 174: 128-32. https://dx.doi.org/10.1016/j.ejogrb.2013.12.014.
  16. Bazot M., Darai E., Hourani R., Thomassin I., Cortez A., Uzan S. et al. Deep pelvic endometriosis: MR imaging for diagnosis and prediction of extension of disease. Radiology. 2004; 232(2): 379-89. https://dx.doi.org/10.1148/radiol.2322030762.
  17. Рухляда Н.Н., Крылов К.Ю. Новые возможности терапии аномальных маточных кровотечений связанных с аденомиозом. Скорая медицинская помощь. 2016; 17(3): 61-4. [Rukhliada N.N., Krylov K.Y. New treatment options for abnormal uterine bleeding associated with adenomyosis. Emergency. 2016; 17(3): 61-4. (in Russian)].
  18. Fanchin R., Ayoubi J.M. Uterine dynamics: impact on the human reproduction process. Reprod. Biomed. Online. 2009; 18(Suppl. 2): 57-62. https://dx.doi.org/10.1016/s1472-6483(10)60450-6.
  19. Youm H.S., Choi Y.S., Han H.D. In vitro fertilization and embryo transfer outcomes in relation to myometrial thickness. J. Assist. Reprod. Genet. 2011; 28(11): 1135-40. https://dx.doi.org/10.1007/s10815-011-9640-7.
  20. 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): 611-8. https://dx.doi.org/10.1111/j.1447-0756.2010.01189.x.
  21. Chiang C.H., Chang M.Y., Shiau C.S., Hou H.C., Hsieh T.T., Soong Y.K. Effect of a sonographically diffusely enlarged uterus without distinct uterine masses on the outcome of in vitro fertilization-embryo transfer. J. Assist. Reprod. Genet. 1999; 16(7): 369-72. https://dx.doi.org/10.1023/a:1020593930366.
  22. Martinez-Conejero J.A., Morgan M., Montesinos M., Fortuno S., Meseguer M., Simon C. et al. Adenomyosis does not affect implantation, but is associated with miscarriage in patients undergoing oocyte donation. Fertil. Steril. 2011; 96(4): 943-50. https://dx.doi.org/10.1016/j.fertnstert.2011.07.1088.
  23. Ballester M., d’Argent E.M., Morcel K., Belaisch-Allart J., Nisolle M., Darai E. Cumulative pregnancy rate after ICSIIVF in patients with colorectal endometriosis: results of a multicentre study. Hum. Reprod. 2012; 27(4):1043-9. https://dx.doi.org/10.1093/humrep/des012.
  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): 62-5. https://dx.doi.org/10.1016/j.ejogrb.2010.02.047.
  25. 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): 273-7. https://dx.doi.org/10.1016/j.rbmo.2012.05.003.
  26. Thalluri V., Tremellen K.P. Ultrasound diagnosed adenomyosis has a negative impact on successful implantation following GnRH antagonist IVF treatment. Hum. Reprod. 2012; 27(12): 3487-92. https://dx.doi.org/10.1093/humrep/des305.
  27. Darai E., Carbonnel M., Dubernard G., Lavoue V., Coutant C., Bazot M. et al. Determinant factors of fertility outcomes after laparoscopic colorectal resection for endometriosis. Eur. J. Obstet. Gynecol. Reprod. Biol. 2010; 149(2): 210-4. https://dx.doi.org/10.1016/j.ejogrb.2009.12.032.
  28. Ferrero S., Anserini P., Abbamonte L.H., Ragni N., Camerini G., Remorgida V. Fertility after bowel resection for endometriosis. Fertil. Steril. 2009; 92(1): 41-6. https://dx.doi.org/10.1016/j.fertnstert.2008.04.070.
  29. Pontis A., D’Alterio M.N., Pirarba S., de Angelis C., Tinelli R., Angioni S. Adenomyosis: a systematic review of medical treatment. Gynecol. Endocrinol. 2016; 32(9): 696-700. https://dx.doi.org/10.1080/09513590.2016.1197200.
  30. Imaoka I., Ascher S.M., Sugimura K., Takahashi K., Li H., Cuomo F. et al. MR imaging of diffuse adenomyosis changes after GnRH analog therapy. J. Magn. Reson. Imaging. 2002; 15(3): 285-90. https://dx.doi.org/10.1002/jmri.10060.
  31. Khan K.N., Kitajima M., Hiraki K., Fujishita A., Nakashima M., Masuzaki H. Decreased expression of human heat shock protein 70 in the endometria and pathological lesions of women with adenomyosis and uterine myoma after GnRH agonist therapy. Eur. J. Obstet. Gynecol. Reprod. Biol. 2015; 187: 6-13. https://dx.doi.org/10.1016/j.ejogrb.2015.01.012.
  32. Niu Z., Chen Q., Sun Y., Feng Y. Long-term pituitary downregulation before frozen embryo transfer could improve pregnancy outcomes in women with adenomyosis. Gynecol. Endocrinol. 2013; 29(12): 1026-30. https://dx.doi.org/10.3109/09513590.2013.824960.
  33. Park C.W., Choi M.H., Yang K.M., Song I.O. Pregnancy rate in women with adenomyosis undergoing fresh or frozen embryo transfer cycles following gonadotropin-releasing hormone agonist treatment. Clin. Exp. Reprod. Med. 2016; 43(3): 169-73. https://dx.doi.org/10.5653/cerm.2016.43.3.169.
  34. Huang X., Huang Q., Chen S., Zhang J., Lin K., Zhang X. Efficacy of laparoscopic adenomyomectomy using double-flap method for diffuse uterine adenomyo-sis. BMC Women’s Health. 2015; 15: 24. https://dx.doi.org/10.1186/s12905-015-0182-5.
  35. Fujishita A., Masuzaki H., Khan K.N., Kitajima M., Ishimaru T. Modified reduction surgery for adenomyosis. A preliminary report of the transverse H incision technique. Gynecol. Obstet. Invest. 2004; 57(3): 132-8. https://dx.doi.org/10.1159/000075830.
  36. Takeuchi H., Kitade M., Kikuchi I., Shimanuki H., Kumakiri J., Kitano T. et al. Laparoscopic adenomyomectomy and hysteroplasty: a novel method. J. Minim. Invasive Gynecol. 2006; 13(2): 150-4. https://dx.doi.org/10.1016/j.jmig.2005.12.004.
  37. Wang P.H., Liu W.M., Fuh J.L., Cheng M.H., Chao H.T. Comparison of surgery alone and combined surgicalmedical treatment in the management of sympto-matic uterine adenomyoma. Fertil. Steril. 2009; 92(3): 876-85. https://dx.doi.org/10.1016/j.fertnstert.2008.07.1744.
  38. Sun A.J., Luo M., Wang W., Chen R., Lang J.H. Characteristics and efficacy of modified adenomyomectomy in the treatment of uterine adenomyoma. Chin. Med. J. (Engl). 2011; 124(9): 1322-6.
  39. Osada H., Silber S., Kakinuma T., Nagaishi M., Kato K., Kato O. Surgical procedure to conserve the uterus for future pregnancy in patients suffering from massive adenomyosis. Reprod. Biomed. Online. 2011; 22(1): 94-9. https://dx.doi.org/10.1016/j.rbmo.2010.09.014.
  40. Saremi A., Bahrami H., Salehian P., Hakak N., Pooladi A. Treatment of adenomyomectomy in women with severe uterine adenomyosis using a novel technique. Reprod. Biomed. Online. 2014; 28(6): 753-60. https://dx.doi.org/10.1016/j.rbmo.2014.02.008.
  41. Huang B.S., Seow K.M., Tsui K.H., Huang C.Y., Lu Y.F., Wang P.H. Fertility outcome of infertile women with adenomyosis treated with the combination of a conservative microsurgical technique and GnRH agonist: long-term follow-up in a series of nine patients. Taiwan. J. Obstet. Gynecol. 2012; 51(2): 212-6. https://dx.doi.org/10.1016/j.tjog.2012.04.008.
  42. Chang W.H., Wang K.C., Lee N.R., Huang N., Su W.H., Chao H.T. et al. Reproductive performance of severely symptomatic women with uterine adenomyoma who wanted preservation of the uterus and underwent combined surgical-medical treatment. Taiwan. J. Obstet. Gynecol. 2013; 52(1): 39-45. https://dx.doi.org/10.1016/j.tjog.2013.01.007.
  43. Wang P.H., Fuh J.L., Chao H.T., Liu W.M., Cheng M.H., Chao K.C. Is the surgical approach beneficial to subfertile women with symptomatic extensive adenomyosis? J. Obstet. Gynaecol. Res. 2009; 35(3): 495-502. https://dx.doi.org/10.1111/j.1447-0756.2008.00951.x.
  44. Grimbizis G.F., Mikos T., Tarlatzis B. Uterus-sparing operative treatment for adenomyosis. Fertil. Steril. 2014; 101(2): 472-87. https://dx.doi.org/10.1016/j.fertnstert.2013.10.025.
  45. Kishi Y., Yabuta M., Taniguchi F. Who will benefit from uterus-sparing surgery in adenomyosis-associated subfertility? Fertil. Steril. 2014; 102(3): 802-7. e1. https://dx.doi.org/10.1016/j.fertnstert.2014.05.028.
  46. Otsubo Y., Nishida M., Arai Y., Ichikawa R., Taneichi A., Sakanaka M. Associ-ation of uterine wall thickness with pregnancy outcome following uterine-sparing surgery for diffuse uterine adenomyosis. Aust. N. Z. J. Obstet. Gynaecol. 2016; 56(1): 88-91. https://dx.doi.org/10.1111/ajo.12419.

Received 06.04.2021

Accepted 08.04.2021

About the Authors

Kirill Yu. Krylov, Ph.D., obstetrician-gynecologist, Senior Researcher at the Department of Gynecology, Saint Petersburg I.I. Dzhanelidze Research Institute of Emergency Medicine. Tel: +7(911)168-70-73. E-mail: drkrylov@mail.ru. ORCID: 0000-0003-2149-5957. 192242, Russia, Saint Petersburg, Budapeshtskaya str., 3А.
Nikolai N. Rukhliada, Dr. Med. Sci., Professor, Head of the Department of Obstetrics and Gynecology, St. Petersburg State Pediatric Medical University,
Ministry of Health of Russia. Tel: +7(911)913-20-20. E-mail: nickolasr@mail.ru. ORCID: 0000-0002-3548-0468. 194100, Russia, Saint Petersburg, Litovskaya str., 2.
Elena I. Birukova, Ph.D., Head of the Department of Gynecology No. 2, Saint Petersburg I.I. Dzhanelidze Research Institute of Emergency Medicine. Tel: +7(911)225-21-31. E-mail: 79112252131@yandex.ru. 192242, Russia, Saint Petersburg, Budapeshtskaya str., 3А.
Leila Sh. Tcechoeva, Ph.D., Head of the Department of Gynecology No. 1, Saint Petersburg I.I. Dzhanelidze Research Institute of Emergency Medicine. Tel: +7(911)163-50-72. E-mail: doctor-leila@mail.ru. 192242, Russia, Saint Petersburg, Budapeshtskaya str., 3А.
Simona V. Vinnikova, postgraduate student of the Department of Obstetrics and Gynecology, St. Petersburg State Pediatric Medical University, Ministry of Health of Russia. Tel: +7(921)571-11-80. E-mail: simona.vinnikova@yandex.ru. 194100, Russia, Saint Petersburg, Litovskaya str., 2.

For citation: Krylov K.Yu., Rukhlyada N.N., Biryukova E.I., Tsechoeva L.Sh., Vinnikova S.V. Hardware visualization of adenomyosis and the reproductive outcomes of surgical treatment for adenomyosis-associated infertility.
Akusherstvo i Ginekologiya/Obstetrics and Gynecology. 2021; 7: 28-36 (in Russian)
https://dx.doi.org/10.18565/aig.2021.7.28-36

Similar Articles

By continuing to use our site, you consent to the processing of cookies that ensure the proper functioning of the site.