Modern approaches to classification of adenomyosis
Maria I. Yarmolinskaya , Maria A. Shalina , Stanislava V. Nagorneva
Journal of obstetrics and women's diseases ›› 2023, Vol. 72 ›› Issue (1) : 97 -108.
Modern approaches to classification of adenomyosis
This article presents a modern review of the main classifications of adenomyosis based on the clinical course, the prevalence of the pathological process, the results of ultrasound and magnetic resonance imaging, and histological verification. The analysis is based on domestic and foreign literature, federal clinical recommendations, and results of our own research. Despite the large number of different classifications of the disease, there are still shortcomings noted in this review. Based on the available rubricators, we emphasized the need to create a classification of adenomyosis with an assessment of the clinical picture, genetic and molecular profiles, the results of non-invasive assessment methods, and a correlation with the histological conclusion. A unified classification would solve many problems in scientific and practical activities for accurate and early diagnosis of adenomyosis, identification of risk groups for patients with an aggressive course of the pathological process, selection of reasonable recommendations, and timely appointment of pathogenetic therapy.
adenomyosis / classification / genital endometriosis / diagnosis
| [1] |
Zhai J, Vannuccini S, Petraglia F, et al. Adenomyosis: mechanisms and pathogenesis. Semin Reprod Med. 2020;38(2−3):129−143. DOI: 10.1055/s-0040-1716687 |
| [2] |
Zhai J., Vannuccini S., Petraglia F., et al. Adenomyosis: mechanisms and pathogenesis // Semin. Reprod. Med. 2020. Vol. 38. No. 2−3. P. 129−143. DOI: 10.1055/s-0040-1716687 |
| [3] |
Habiba M, Benagiano G, Brosens I. The pathophysiology of adenomyosis. In: Uterine adenomyosis. Ed. by M. Habiba, G. Benagiano. Heidelberg: Springer; 2016: 45–70. |
| [4] |
Habiba M., Benagiano G., Brosens I. The pathophysiology of adenomyosis. In: Uterine Adenomyosis / Ed. by M. Habiba, G. Benagiano. Heidelberg: Springer, 2016. P. 45–70. |
| [5] |
The international statistical classification of diseases and related health problems. 11th revision (ICD-11). (In Russ.). [cited 2022 Dec 21]. Available from: https://mkb11.online/ |
| [6] |
Международная статистическая классификация болезней и проблем, связанных со здоровьем. Одиннадцатый пересмотр (МКБ-11). Москва, 2022 [дата обращения 21.12.2022]. Доступ по ссылке: https://mkb11.online/ |
| [7] |
Yarmolinskaya MI, Aylamazyan EK. Genital’nyy endometrioz. Razlichnye grani problemy. Saint Petersburg: Eco-Vector; 2017. (In Russ.). |
| [8] |
Ярмолинская М.И., Айламазян Э.К. Генитальный эндометриоз. Различные грани проблемы. Санкт-Петербург: Эко-Вектор, 2017. |
| [9] |
Aylamazyan EK, Yarmolinskaya MI, Molotkov AS, et al. Classifications of endometriosis. Journal of Obstetrics and Women’s Diseases. 2017;66(2):77–92. (In Russ.). DOI: 10.17816/JOWD66277-92 |
| [10] |
Айламазян Э.К., Ярмолинская М.И., Молотков А.С., и др. Классификации эндометриоза // Журнал акушерства и женских болезней. 2017. Т. 66. № 2. C. 77−92. DOI: 10.17816/JOWD66277-92 |
| [11] |
Endometrioz. Klinicheskie rekomendatsii / OOO “Rossiyskoe obshchestvo akusherov-ginekologov” (ROAG), MZ RF. Moscow, 2020: 42. (In Russ.). [cited 2022 Dec 21]. Available from: https://minzdrav.permkrai.ru/dokumenty/153568/ |
| [12] |
Эндометриоз. Клинические рекомендации / ООО «Российское общество акушеров-гинекологов» (РОАГ), МЗ РФ. Москва, 2020 [дата обращения 21.12.2022]. Доступ по ссылке: https://minzdrav.permkrai.ru/dokumenty/153568/ |
| [13] |
Adamjan LV, Kulakov VI. Endometriozy. Moscow: Medicina; 1998. (In Russ.). |
| [14] |
Адамян Л.В., Кулаков В.И. Эндометриозы: руководство для врачей. Москва: Медицина, 1998. |
| [15] |
Gordts S, Grimbizis G, Campo R. Symptoms and classification of uterine adenomyosis, including the place of hysteroscopy in diagnosis. Fertil Steril. 2018;109(3):380–388. DOI: 10.1016/j.fertnstert.2018.01.006 |
| [16] |
Gordts S., Grimbizis G., Campo R. Symptoms and classification of uterine adenomyosis, including the place of hysteroscopy in diagnosis // Fertil. Steril. 2018. Vol. 109. No. 3. P. 380−388. DOI: 10.1016/j.fertnstert.2018.01.006 |
| [17] |
Tskhay VB. Adenomioz. Kontraversii sovremennosti. Boli. Krovotecheniya. Besplodie. Ed. by V.E. Radzinskiy. Moscow: StatusPraeses; 2020. (In Russ.). |
| [18] |
Цхай В. Б. Аденомиоз. Контраверсии современности. Боли. Кровотечения. Бесплодие / под ред. В.Е. Радзинского. Москва: StatusPraeses, 2020. |
| [19] |
Van den Bosch T, Dueholm M, Leone FP, 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 Obstet Gynecol. 2015;46(3):284–298. DOI: 10.1002/uog.14806 |
| [20] |
Van den Bosch T., Dueholm M., Leone F.P., 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 Obstet. Gynecol. 2015 Vol. 46. No. 3. P. 284-298. DOI: 10.1002/uog.14806 |
| [21] |
Pistofidis G, Makrakis E, Koukoura O, et al. Distinct types of uterine adenomyosis based on laparoscopic and histopathologic criteria. Clin Exp Obstet Gynecol. 2014;41(2):113–118. |
| [22] |
Pistofidis G., Makrakis E., Koukoura O., et al. Distinct types of uterine adenomyosis based on laparoscopic and histopathologic criteria // Clin. Exp. Obstet. Gynecol. 2014. Vol. 41. No. 2. P. 113−118. |
| [23] |
Brosens I, Gordts S, Habiba M, et al. Uterine cystic adenomyosis: a disease of younger women. J PediatrAdolesc Gynecol. 2015;28(6):420–426. DOI: 10.1016/j.jpag.2014.05.008 |
| [24] |
Brosens I., Gordts S., Habiba M., et al. Uterine cystic adenomyosis: a disease of younger women // J. Pediatr. Adolesc. Gynecol. 2015. Vol. 28. No. 6. P. 420−426. DOI: 10.1016/j.jpag.2014.05.008 |
| [25] |
Koukoura O, Kapsalaki E, Daponte A, et al. Laparoscopic treatment of a large uterine cystic adenomyosis in a young patient. BMJ Case Rep. 2015;2015. DOI: 10.1136/bcr-2015-210358 |
| [26] |
Koukoura O., Kapsalaki E., Daponte A., et al. Laparoscopic treatment of a large uterine cystic adenomyosis in a young patient // BMJ Case Rep. 2015. Vol. 2015. DOI: 10.1136/bcr-2015-210358 |
| [27] |
Grimbizis GF, Mikos T, Tarlatzis B. Uterus-sparing operative treatment for adenomyosis. Fertil Steril. 2014;101(2):472–487. DOI: 10.1016/j.fertnstert.2013.10.025 |
| [28] |
Grimbizis G.F., Mikos T., Tarlatzis B. Uterus-sparing operative treatment for adenomyosis // Fertil. Steril. 2014. Vol. 101. No. 2. P. 472−487. DOI: 10.1016/j.fertnstert.2013.10.025 |
| [29] |
Yarmolinskaya MI, Ailamazyan EK, Arutyunyan AF, et al. Sclerotic adenomyosis: a case report. Journal of Obstetrics and Women’s Diseases. 2018;67(6):119–123. (In Russ.). DOI: 10.17816/JOWD676119-123 |
| [30] |
Ярмолинская М.И., Айламазян Э.К., Арутюнян А.Ф., и др. Склеротическая форма аденомиоза (описание клинического случая) // Журнал акушерства и женских болезней. 2018. Т. 67. № 6. C. 119−123. DOI: 10.17816/JOWD676119-123 |
| [31] |
Kishi Y, Suginami H, Kuramori R, et al. Four subtypes of adenomyosis assessed by magnetic resonance imaging and their specification. Am J Obstet Gynecol. 2012;207(2):114.e1−114.e1147. DOI: 10.1016/j.ajog.2012.06.027 |
| [32] |
Kishi Y., Suginami H., Kumamori R., et al. Four subtypes of adenomyosis assessed by magnetic resonance imaging and their specification // Am. J. Obstet. Gynecol. 2012. Vol. 207. P. 114.e1–114.e7. DOI: 10.1016/j.ajog.2012.06.027 |
| [33] |
Bourdon M, Oliveira J, Marcellin L, et al. Adenomyosis of the inner and outer myometrium are associated with different clinical profiles. Hum Reprod. 2021;36(2):349–357. DOI: 10.1093/humrep/deaa307 |
| [34] |
Bourdon M., Oliveira J., Marcellin L., et al. Adenomyosis of the inner and outer myometrium are associated with different clinical profiles // Hum. Reprod. 2021. Vol. 36. No. 2. P. 349−357. DOI: 10.1093/humrep/deaa307 |
| [35] |
Khan KN, Fujishita A, Mori T. Pathogenesis of human adenomyosis: current understanding and its association with infertility. J Clin Med. 2022;11(14). DOI: 10.3390/jcm11144057 |
| [36] |
Khan K.N., Fujishita A., Mori T. Pathogenesis of human adenomyosis: current understanding and its association with infertility // J. Clin. Med. 2022. Vol. 11. No. 14. DOI: 10.3390/jcm11144057 |
| [37] |
Brosens JJ, de Souza NM, Barker FG. Uterine junctional zone: function and disease. Lancet. 1995;346:558–560. DOI: 10.1016/S0140-6736(95)91387-4 |
| [38] |
Brosens J.J., de Souza N.M., Barker F.G. Uterine junctional zone: function and disease // Lancet. 1995. Vol. 346. P. 558–560. DOI: 10.1016/S0140-6736(95)91387-4 |
| [39] |
Naftalin J, Jurkovic D. The endometrial-myometrial junction: a fresh look at a busy crossing. Ultrasound Obstet Gynecol. 2009;34:1–11. DOI: 10.1002/uog.6432 |
| [40] |
Naftalin J., Jurkovic D. The endometrial-myometrial junction: a fresh look at a busy crossing // Ultrasound Obstet. Gynecol. 2009. Vol. 34. P. 1–11. DOI: 10.1002/uog.6432 |
| [41] |
Zhang Y, Zhou L, Li TC, et al. Ultrastructural features of endometrial-myometrial interface and its alteration in adenomyosis. Int J Clin Exp Pathol. 2014;7:1469–1477. |
| [42] |
Zhang Y., Zhou L., Li T.C., et al. Ultrastructural features of endometrial-myometrial interface and its alteration in adenomyosis // Int. J. Clin. Exp. Pathol. 2014. Vol. 7. P. 1469–1477. |
| [43] |
Chapron C, Tosti C, Marcellin L, et al. Relationship between the magnetic resonance imaging appearance of adenomyosis and endometriosis phenotypes. Hum Reprod. 2017;32:1393–1401. DOI: 10.1093/humrep/dex088 |
| [44] |
Chapron C., Tosti C., Marcellin L., et al. Relationship between the magnetic resonance imaging appearance of adenomyosis and endometriosis phenotypes // Hum. Reprod. 2017. Vol. 32. P. 1393–1401. DOI: 10.1093/humrep/dex088 |
| [45] |
Khan KN, Fujishita A, Koshiba A, et al. Biological differences between intrinsic and extrinsic adenomyosis with coexisting deep infiltrating endometriosis. Reprod Biomed Online. 2019; 39(2):343–353. DOI: 10.1016/j.rbmo.2019.03.210 |
| [46] |
Khan K.N., Fujishita A., Koshiba A., et al. Biological differences between intrinsic and extrinsic adenomyosis with coexisting deep infiltrating endometriosis // Reprod. Biomed. Online. 2019. Vol. 39. No. 2. P. 343−353. DOI: 10.1016/j.rbmo.2019.03.210 |
| [47] |
Tuttlies F, Keckstein J, Ulrich U, et al. ENZIAN-score, a classification of deep infiltrating endometriosis. Zentralbl Gynakol. 2005;127:275–281. DOI: 10.1055/s-2005-836904 |
| [48] |
Tuttlies F., Keckstein J., Ulrich U., et al. ENZIAN-score, a classification of deep infiltrating endometriosis // Zentralbl. Gynakol. 2005. No. 127. P. 275−281. DOI: 10.1055/s-2005-836904 |
| [49] |
Bazot M, Darai E. Role of transvaginal sonography and magnetic resonance imaging in the diagnosis of uterine adenomyosis. Fertil Steril. 2018;109:389–397. DOI: 10.1016/j.fertnstert.2018.01.024 |
| [50] |
Bazot M., Darai E. Role of transvaginal sonography and magnetic resonance imaging in the diagnosis of uterine adenomyosis // Fertil. Steril. 2018. Vol. 109. P. 389–397. DOI: 10.1016/j.fertnstert.2018.01.024 |
| [51] |
Vercellini P, Vigano P, Somigliana E, et al. Adenomyosis: epidemiological factors. Best Pract Res Clin Obstet Gynaecol. 2006;20(4):465–477. DOI: 10.1016/j.bpobgyn.2006.01.017 |
| [52] |
Vercellini P., Vigano P., Somigliana E., et al. Adenomyosis: epidemiological factors // Best. Pract. Res. Clin. Obstet. Gynaecol. 2006 Vol. 20. No. 4. P. 465–477. DOI: 10.1016/j.bpobgyn.2006.01.017 |
| [53] |
Bromley B, Shipp TD, Benacerraf B. Adenomyosis: sonographic findings and diagnostic accuracy. J Ultrasound Med. 2000;19(8):529–534. DOI: 10.7863/jum.2000.19.8.529 |
| [54] |
Bromley B., Shipp T. D., Benacerraf B. Adenomyosis: sonographic findings and diagnostic accuracy // J. Ultrasound. Med. 2000. Vol. 19. No. 8. P. 529–534. DOI: 10.7863/jum.2000.19.8.529 |
| [55] |
Vannuccini S, Petraglia F. Recent advances in understanding and managing adenomyosis. F1000Res. 2019;8. DOI: 10.12688/f1000research.17242.1 |
| [56] |
Vannuccini S., Petraglia F. Recent advances in understanding and managing adenomyosis. F1000Res. 2019. Vol. 8. DOI: 10.12688/f1000research.17242.1 |
| [57] |
Patent RUS No. 2764106 / 13.01.2022 Byul. No. 2 Nagorneva SV, Shalina MA, Yarmolinskaya MI, et al. Sposob diagnostiki adenomioza. (In Russ.). [cited 2022 Dec 21]. Available from: https://patenton.ru/patent/RU2764106C1.pdf |
| [58] |
Патент РФ на изобретение № 2764106 / 13.01.2022 Бюл. № 2 Нагорнева С.В., Шалина М.А., Ярмолинская М.И., и др. Способ диагностики аденомиоза [дата обращения 21.12.2022]. Доступно по ссылке: https://patenton.ru/patent/RU2764106C1.pdf |
| [59] |
Nagorneva SV, Shalina MA, Yarmolinskaya MI, et al. Comprehensive method of ultrasound diagnosis of adenomyosis. Journal of Obstetrics and Women’s Diseases. 2021;70(6):73–82. DOI: 10.17816/JOWD83066 |
| [60] |
Нагорнева С.В., Шалина М.А., Ярмолинская М.И., и др. Комплексная методика ультразвуковой диагностики аденомиоза // Журнал акушерства и женских болезней. 2021. Т. 70. № 6. C. 73–82. DOI: 10.17816/JOWD83066 |
| [61] |
Tamai K, Togashi K, Ito T, et al. MR imaging findings of adenomyosis: correlation with histopathologic features and diagnostic pitfalls. Radiographics. 2005;25(1):21−40. DOI: 10.1148/rg.251045060 |
| [62] |
Tamai K., Togashi K., Ito T., et al. MR imaging findings of adenomyosis: correlation with histopathologic features and diagnostic pitfalls // Radiographics. 2005. Vol. 25. No. 1. P. 21–40. DOI: 10.1148/rg.251045060 |
| [63] |
Exacoustos C, Manganaro L, Zupi E. Imaging for the evaluation of endometriosis and adenomyosis. Best Pract Res Clin Obstet Gynaecol. 2014;28(5):655–681. DOI: 10.1016/j.bpobgyn.2014.04.010 |
| [64] |
Exacoustos C., Manganaro L., Zupi E. Imaging for the evaluation of endometriosis and adenomyosis // Best. Pract. Res. Clin. Obstet. Gynaecol. 2014. Vol. 28. No. 5. P. 655–681. DOI: 10.1016/j.bpobgyn.2014.04.010 |
| [65] |
Champaneria R, Abedin P, Daniels J, et al. 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. DOI: 10.3109/00016349.2010.512061 |
| [66] |
Champaneria R., Abedin P., Daniels J., et al. Ultrasound scan and magnetic resonance imaging for the diagnosis of adenomyosis: systematic review comparing test accuracy // Acta Obstet. Gynecol. Scand. 2010. Vol. 89. No. 11. P. 1374–1384. DOI: 10.3109/00016349.2010.512061 |
| [67] |
Kunz G, Beil D, Huppert P, et al. Adenomyosis in endometriosis-prevalence and impact on fertility. Evidence from magnetic resonance imaging. Hum Reprod. 2005;20:2309–2316. DOI: 10.1093/humrep/dei021 |
| [68] |
Kunz G., Beil D., Huppert P., et al. Adenomyosis in endometriosis-prevalence and impact on fertility. Evidence from magnetic resonance imaging // Hum. Reprod. 2005. Vol. 20. P. 2309–2316. DOI: 10.1093/humrep/dei021 |
| [69] |
Khan KN, Fujishita A, Kitajima M, et al. Biological differences between functionalis and basalis endometria in women with and without adenomyosis. Eur J Obstet Gynecol Reprod Biol. 2016;203:49–55. DOI: 10.1016/j.ejogrb.2016.05.012 |
| [70] |
Khan K.N., Fujishita A., Kitajima M., et al. Biological differences between functionalis and basalis endometria in women with and without adenomyosis // Eur. J. Obstet. Gynecol. Reprod. Biol. 2016. Vol. 203. P. 49–55. DOI: 10.1016/j.ejogrb.2016.05.012 |
| [71] |
Gordts S, Brosens JJ, Fusi L, et al. Uterine adenomyosis: a need for uniform terminology and consensus classification. Reprod Biomed Online. 2008;17(2):244–248. DOI: 10.1016/s1472-6483(10)60201-5 |
| [72] |
Gordts S., Brosens J.J., Fusi L. et al. Uterine adenomyosis: a need for uniform terminology and consensus classification // Reprod. Biomed. Online. 2008. Vol. 17. No. 2. P. 244–248. DOI: 10.1016/s1472-6483(10)60201-5 |
| [73] |
Kobayashi H, Matsubara S. A classification proposal for adenomyosis based on magnetic resonance imaging. Gynecol Obstet Invest. 2020;85(2):118–126. DOI: 10.1159/000505690 |
| [74] |
Kobayashi H., Matsubara S. A classification proposal for adenomyosis based on magnetic resonance imaging // Gynecol. Obstet. Invest. 2020. Vol. 85. No. 2. P. 118–126. DOI: 10.1159/000505690 |
| [75] |
Novellas S, Chassang M, Delotte J, et al. MRI characteristics of the uterine junctional zone: From normal to the diagnosis of adenomyosis. Am J Roentgenol. 2011;196(5):1206–1213. DOI: 10.2214/AJR.10.4877 |
| [76] |
Novellas S., Chassang M., Delotte J., et al. MRI characteristics of the uterine junctional zone: From normal to the diagnosis of adenomyosis // Am. J. Roentgenol. 2011. Vol. 196. No. 5. P. 1206–1213. DOI: 10.2214/AJR.10.4877 |
| [77] |
Togashi K, Kawakami S, Kimura I, et al. Uterine contractions: possible diagnostic pitfall at MR imaging. J MagnReson Imaging. 1993;3(6):889–893. DOI: 10.1002/jmri.1880030616 |
| [78] |
Togashi K., Kawakami S., Kimura I., et al. Uterine contractions: possible diagnostic pitfall at MR imaging // J. Magn. Reson. Imaging. 1993. Vol. 3. No. 6. P. 889–893. DOI: 10.1002/jmri.1880030616 |
| [79] |
Zheleznov BI, Strizhakov AN. Genital’nyy endometrioz. Moscow: Meditsina. 1985. (In Russ.). |
| [80] |
Железнов Б.И., Стрижаков А.Н. Генитальный эндометриоз. Москва: Медицина, 1985. |
| [81] |
Donnez J, Donnez O, Dolmans MM. Introduction: uterine adenomyosis, another enigmatic disease of our time. Fertil Steril. 2018;109(3):369–370. DOI: 10.1016/j.fertnstert.2018.01.035 |
| [82] |
Donnez J., Donnez O., Dolmans M.M. Introduction: uterine adenomyosis, another enigmatic disease of our time // Fertil. Steril. 2018. Vol. 109. No. 3. P. 369–370. DOI: 10.1016/j.fertnstert.2018.01.035 |
Eсо-Vector
/
| 〈 |
|
〉 |