MRI Features of Malignant Transformation of Pelvic Endometriosis: A Systematic Review
-
Behnaz Moradi
,
Masoumeh Gity
,
Sara Hassani
,
Mobin Azami
,
Maryam Rahmani
,
Fahimeh Azizi Nik
,
Arash Khameneh Bagheri
,
Shirin Yaghoobpoor
,
Hamed Ghorani
Abstract
Background: Endometriosis is a benign gynecologic condition that is estrogen-dependent. Malignant transformation is one of the complications of endometriosis; it can affect the woman's ovarian and extra-ovarian regions. Diagnosing endometriosis-associated cancers has an essential role in treatment. Purpose: Our study aimed to review magnetic resonance imaging (MRI) features of malignant transformation of pelvic endometriosis. Material and Methods: We searched three online databases including Web of Science, Scopus, and PubMed, applying relevant keywords up to May 2022. We included English articles reporting MRI features of pelvic endometriosis pointing to malignant transformation. Results: Totally eight papers were included as they matched our inclusion requirements. Eighty-seven individuals were included finally. Studies were published between 1992 and 2021. The larger size of the lesion, loss of T2-weighted images shading, mural nodules, mural nodules contrast enhancement, and mural nodules protruding from the cyst wall at acute angles were the main MRI features suggesting potential malignant transformation of pelvic endometriosis. Conclusion: The endometriosis's malignant changes can be observed on MRI. The predominant MRI findings are a large cyst, loss of shading on T2-weighted imaging, mural nodules enhancement, and acutely angled protrusion of mural nodules from the cyst wall.
References
1. Vercellini P, Viganò P, Somigliana E, et al. Endometriosis: pathogenesis and treatment. Nat Rev Endocrinol 2014;10:261-275.
2. Burney RO, Giudice LC. Pathogenesis and pathophysiology of endometriosis. Fertil Steril 2012;98:511-519.
3. Kvaskoff M,1 Mahamat-Saleh Y, Farland LV, et al. Endometriosis and cancer: a systematic review and meta-analysis. Hum Reprod Update 2021;27:393-420.
4. Eskenazi B, Warner ML. Epidemiology of endometriosis. Obstet Gynecol Clin N Am 1997;24:235-258.
5. Bulletti C, Coccia ME, Battistoni S, et al. Endometriosis and infertility. J Assist Reprod Genet 2010;27:441-447.
6. Parasar P, Ozcan P, Terry KL. Endometriosis: epidemiology, diagnosis and clinical management. Curr Obstet Gynecol 2017;6:34-41.
7. Neto JS, Kho RM, dos Santos Siufi DF, et al, histologic, and molecular changes associated with endometriosis and ovarian cancer. J Minim Invasive Gynecol 2014;21:55-63.
8. Koninckx PR, Muyldermans M, Moerman P, et al. CA 125 concentrations in ovarian ‘chocolate’cyst fluid can differentiate an endometriotic cyst from a cystic corpus luteum. Hum Reprod 1992;7:1314-1317.
9. Munksgaard PS, Blaakaer J. The association between endometriosis and ovarian cancer: a review of histological, genetic and molecular alterations. Gynecol Oncol 2012;124:164-169.
10. Kok VC, Tsai H-J, Su C-F, et al. The risks for ovarian, endometrial, breast, colorectal, and other cancers in women with newly diagnosed endometriosis or adenomyosis: a population-based study. Int J Gynecol Cancer 2015;25:1.
11. Heaps JM, Nieberg RK, Berek JS. Malignant neoplasms arising in endometriosis. Obstet Gynecol 1990;75:1023-1028.
12. Scully RE, Richardson GS, Barlow JF. The development of malignancy in endometriosis. Clin Obstet Gynecol 1966;9:384-411.
13. Scully RE, Barlow JF. “Mesonephroma” of ovary. Tumor of müllerian nature related to the endometrioid carcinoma. Cancer 1967;20:1405-1417.
14. Leiserowitz GS, Gumbs JL, Oi R, et al. Endometriosis-related malignancies. Int J Gynecol Cancer 2003;13:1.
15. McDermott S, Oei TN, Iyer VR, et al. MR imaging of malignancies arising in endometriomas and extraovarian endometriosis. Radiographics 2012;32:845-863.
16. Tanaka YO, Yoshizako T, Nishida M, et al. Ovarian carcinoma in patients with endometriosis: MR imaging findings. AJR 2000;175:1423-1430.
17. Siegelman ES, Outwater E, Wang T, et al. Solid pelvic masses caused by endometriosis: MR imaging features. AJR 1994;163:357-361.
18. Tanaka YO, Okada S, Yagi T, et al. MRI of endometriotic cysts in association with ovarian carcinoma. AJR 2010;194:355-361.
19. Bourgioti C, Preza O, Panourgias E, et al. MR imaging of endometriosis: Spectrum of disease. Diagn Interv Imaging 2017;98:751-767.
20. Sampson JA. Endometrial carcinoma of the ovary, arising in endometrial tissue in that organ. Arch Surg 1925;10:1-72.
21. Stringfellow JM, Hawnaur JM. CT and MRI appearances of sarcomatous change in chronic pelvic endometriosis. Brit J Radiol 1998;71:90-93.
22. Wang D, Yang Q, Wang H, et al. Malignant transformation of hepatic endometriosis: a case report and literature review. BMC women's health. 2021;21:1-7.
23. Matsubara S, Kawahara N, Horie A, et al. Magnetic resonance relaxometry improves the accuracy of conventional MRI in the diagnosis of endometriosis‑associated ovarian cancer: A case report. Mol Clin Oncol 2019;11:296-300.
24. N'Senda P, Wendum D, Balladur P, et al. Adenosarcoma arising in hepatic endometriosis. Eur Radiol 2000;10:1287-1289.
25. Song L, Xing A, Li Q, et al. High-Grade Serous Carcinoma Resulting From Rectal Endometriosis and Complicated With Ovarian Cancer. Front Oncol 2019;9:1252.
26. Grasso RF, Del Vescovo R, Cazzato RL, et al. Pelvic endometriosis: A mr pictorial review. endometriosis-basic concepts and current research trends InTech Open Access Publisher. 2012:447-458.
27. Corwin MT, Gerscovich EO, Lamba R, et al. Differentiation of ovarian endometriomas from hemorrhagic cysts at MR imaging: utility of the T2 dark spot sign. Radiology 2014;271:126-132.
28. Woodward PJ, Sohaey R, Mezzetti TP, et al: radiologic-pathologic correlation. Radiographics 2001;21:193-216; questionnaire 88-94.
29. Benoit L, Arnould L, Cheynel N, et al. Malignant extraovarian endometriosis: a review. EJSO 2006;32:6-11.
30. Brooks JJ, Wheeler JE. Malignancy arising in extragonadal endometriosis. A case report and summary of the world literature. Cancer 1977;40:3065-3073.
31. Modesitt SC, Tortolero-Luna G, Robinson JB, et al. Ovarian and extraovarian endometriosis-associated cancer. Obstet Gynecol 2002;100:788-795.
32. Clement PB. The pathology of endometriosis: a survey of the many faces of a common disease emphasizing diagnostic pitfalls and unusual and newly appreciated aspects. Adv Anat Pathol 2007;14:241-260.
33. Chamié LP, Blasbalg R, Gonçalves MO, et al. Accuracy of magnetic resonance imaging for diagnosis and preoperative assessment of deeply infiltrating endometriosis. Int J Gynaecol Obstet 2009;106:198-201.
34. Sala E, Rockall A, Rangarajan D, et al. The role of dynamic contrast-enhanced and diffusion weighted magnetic resonance imaging in the female pelvis. Eur J Radiol 2010;76:367-385.
35. Coutinho AC, Krishnaraj A, Pires CE, et al. Pelvic applications of diffusion magnetic resonance images. Magn Reson Imaging Clin 2011;19:133-157.
36. Takeuchi M, Matsuzaki K, Uehara H, et al. Malignant transformation of pelvic endometriosis: MR imaging findings and pathologic correlation. Radiographics 2006;26:407-417.
37. Eržen M, Rakar S, Klančar B, et al. Endometriosis-associated ovarian carcinoma (EAOC): an entity distinct from other ovarian carcinomas as suggested by a nested case-control study. Gynecol Oncol 2001;83:100-108.
38. Nyberg DA, Porter BA, Olds MO, et al. MR imaging of hemorrhagic adnexal masses. JCAT 1987;11:664-669.
39. Ja S. Perforating hemorrhagic (chocolate) cysts of the ovary; Their importance and specially their relation to pelvic adenomas of the endometrorial type. Arch Surg 1921;3:245-323.
40. Choudhary S, Fasih N, Papadatos D, et al. Unusual imaging appearances of endometriosis. AJR 2009;192:1632-1644.
41. Saba L, Sulcis R, Melis GB, et al. Endometriosis: the role of magnetic resonance imaging. Acta Radiol 2015;56:355-367.
42. Del Frate C, Girometti R, Pittino M, et al. Deep retroperitoneal pelvic endometriosis: MR imaging appearance with laparoscopic correlation. Radiographics 2006;26:1705-1718.
43. Iwamoto H, Suzuki M, Watanabe N, et al. Case study of a pregnant woman with decidualized ovarian endometriosis whose preoperative findings suggested malignant transformation. Eur J Gynaecol Oncol 2006;27:301-303.
44. Sammour RN, Leibovitz Z, Shapiro I, et al. Decidualization of ovarian endometriosis during pregnancy mimicking malignancy. J Ultrasound Med 2005;24:1289-1294.
45. Machida S, Matsubara S, Ohwada M, et al. Decidualization of ovarian endometriosis during pregnancy mimicking malignancy: report of three cases with a literature review. Gynecol Obstet Invest 2008;66:241-247.
46. Miyakoshi K, Tanaka M, Gabionza D, et al. Decidualized ovarian endometriosis mimicking malignancy. AJR 1998;171:1625-1626.
47. Yoshida S, Onogi A, Shigetomi H, et al. Two cases of pregnant women with ovarian endometrioma mimicking a malignant ovarian tumor. J Clin Ultrasound 2008;36:512-516.
48. Barbieri M, Somigliana E, Oneda S, et al. Decidualized ovarian endometriosis in pregnancy: a challenging diagnostic entity. Hum Reprod 2009;24:1818-1824.
49. Takeuchi M, Matsuzaki K, Nishitani H. Magnetic resonance manifestations of decidualized endometriomas during pregnancy. J Comput Assist Tomogr 2008;32:353-355.
50. Stringfellow JM, Hawnaur JM. CT and MRI appearances of sarcomatous change in chronic pelvic endometriosis. Brit J Radiol 1998;71:90-93.
51. Song L, Xing A, Li Q, Wang G. High-Grade Serous Carcinoma Resulting From Rectal Endometriosis and Complicated With Ovarian Cancer. Front Oncol 2019;9.
52. Matsubara S, Kawahara N, Horie A, et al. Magnetic resonance relaxometry improves the accuracy of conventional MRI in the diagnosis of endometriosis-associated ovarian cancer: A case report. Mol Clin Oncol 2019;11:296-300.
1. Vercellini P, Viganò P, Somigliana E, et al. Endometriosis: pathogenesis and treatment. Nat Rev Endocrinol 2014;10:261-275.
2. Burney RO, Giudice LC. Pathogenesis and pathophysiology of endometriosis. Fertil Steril 2012;98:511-519.
3. Kvaskoff M,1 Mahamat-Saleh Y, Farland LV, et al. Endometriosis and cancer: a systematic review and meta-analysis. Hum Reprod Update 2021;27:393-420.
4. Eskenazi B, Warner ML. Epidemiology of endometriosis. Obstet Gynecol Clin N Am 1997;24:235-258.
5. Bulletti C, Coccia ME, Battistoni S, et al. Endometriosis and infertility. J Assist Reprod Genet 2010;27:441-447.
6. Parasar P, Ozcan P, Terry KL. Endometriosis: epidemiology, diagnosis and clinical management. Curr Obstet Gynecol 2017;6:34-41.
7. Neto JS, Kho RM, dos Santos Siufi DF, et al, histologic, and molecular changes associated with endometriosis and ovarian cancer. J Minim Invasive Gynecol 2014;21:55-63.
8. Koninckx PR, Muyldermans M, Moerman P, et al. CA 125 concentrations in ovarian ‘chocolate’cyst fluid can differentiate an endometriotic cyst from a cystic corpus luteum. Hum Reprod 1992;7:1314-1317.
9. Munksgaard PS, Blaakaer J. The association between endometriosis and ovarian cancer: a review of histological, genetic and molecular alterations. Gynecol Oncol 2012;124:164-169.
10. Kok VC, Tsai H-J, Su C-F, et al. The risks for ovarian, endometrial, breast, colorectal, and other cancers in women with newly diagnosed endometriosis or adenomyosis: a population-based study. Int J Gynecol Cancer 2015;25:1.
11. Heaps JM, Nieberg RK, Berek JS. Malignant neoplasms arising in endometriosis. Obstet Gynecol 1990;75:1023-1028.
12. Scully RE, Richardson GS, Barlow JF. The development of malignancy in endometriosis. Clin Obstet Gynecol 1966;9:384-411.
13. Scully RE, Barlow JF. “Mesonephroma” of ovary. Tumor of müllerian nature related to the endometrioid carcinoma. Cancer 1967;20:1405-1417.
14. Leiserowitz GS, Gumbs JL, Oi R, et al. Endometriosis-related malignancies. Int J Gynecol Cancer 2003;13:1.
15. McDermott S, Oei TN, Iyer VR, et al. MR imaging of malignancies arising in endometriomas and extraovarian endometriosis. Radiographics 2012;32:845-863.
16. Tanaka YO, Yoshizako T, Nishida M, et al. Ovarian carcinoma in patients with endometriosis: MR imaging findings. AJR 2000;175:1423-1430.
17. Siegelman ES, Outwater E, Wang T, et al. Solid pelvic masses caused by endometriosis: MR imaging features. AJR 1994;163:357-361.
18. Tanaka YO, Okada S, Yagi T, et al. MRI of endometriotic cysts in association with ovarian carcinoma. AJR 2010;194:355-361.
19. Bourgioti C, Preza O, Panourgias E, et al. MR imaging of endometriosis: Spectrum of disease. Diagn Interv Imaging 2017;98:751-767.
20. Sampson JA. Endometrial carcinoma of the ovary, arising in endometrial tissue in that organ. Arch Surg 1925;10:1-72.
21. Stringfellow JM, Hawnaur JM. CT and MRI appearances of sarcomatous change in chronic pelvic endometriosis. Brit J Radiol 1998;71:90-93.
22. Wang D, Yang Q, Wang H, et al. Malignant transformation of hepatic endometriosis: a case report and literature review. BMC women's health. 2021;21:1-7.
23. Matsubara S, Kawahara N, Horie A, et al. Magnetic resonance relaxometry improves the accuracy of conventional MRI in the diagnosis of endometriosis‑associated ovarian cancer: A case report. Mol Clin Oncol 2019;11:296-300.
24. N'Senda P, Wendum D, Balladur P, et al. Adenosarcoma arising in hepatic endometriosis. Eur Radiol 2000;10:1287-1289.
25. Song L, Xing A, Li Q, et al. High-Grade Serous Carcinoma Resulting From Rectal Endometriosis and Complicated With Ovarian Cancer. Front Oncol 2019;9:1252.
26. Grasso RF, Del Vescovo R, Cazzato RL, et al. Pelvic endometriosis: A mr pictorial review. endometriosis-basic concepts and current research trends InTech Open Access Publisher. 2012:447-458.
27. Corwin MT, Gerscovich EO, Lamba R, et al. Differentiation of ovarian endometriomas from hemorrhagic cysts at MR imaging: utility of the T2 dark spot sign. Radiology 2014;271:126-132.
28. Woodward PJ, Sohaey R, Mezzetti TP, et al: radiologic-pathologic correlation. Radiographics 2001;21:193-216; questionnaire 88-94.
29. Benoit L, Arnould L, Cheynel N, et al. Malignant extraovarian endometriosis: a review. EJSO 2006;32:6-11.
30. Brooks JJ, Wheeler JE. Malignancy arising in extragonadal endometriosis. A case report and summary of the world literature. Cancer 1977;40:3065-3073.
31. Modesitt SC, Tortolero-Luna G, Robinson JB, et al. Ovarian and extraovarian endometriosis-associated cancer. Obstet Gynecol 2002;100:788-795.
32. Clement PB. The pathology of endometriosis: a survey of the many faces of a common disease emphasizing diagnostic pitfalls and unusual and newly appreciated aspects. Adv Anat Pathol 2007;14:241-260.
33. Chamié LP, Blasbalg R, Gonçalves MO, et al. Accuracy of magnetic resonance imaging for diagnosis and preoperative assessment of deeply infiltrating endometriosis. Int J Gynaecol Obstet 2009;106:198-201.
34. Sala E, Rockall A, Rangarajan D, et al. The role of dynamic contrast-enhanced and diffusion weighted magnetic resonance imaging in the female pelvis. Eur J Radiol 2010;76:367-385.
35. Coutinho AC, Krishnaraj A, Pires CE, et al. Pelvic applications of diffusion magnetic resonance images. Magn Reson Imaging Clin 2011;19:133-157.
36. Takeuchi M, Matsuzaki K, Uehara H, et al. Malignant transformation of pelvic endometriosis: MR imaging findings and pathologic correlation. Radiographics 2006;26:407-417.
37. Eržen M, Rakar S, Klančar B, et al. Endometriosis-associated ovarian carcinoma (EAOC): an entity distinct from other ovarian carcinomas as suggested by a nested case-control study. Gynecol Oncol 2001;83:100-108.
38. Nyberg DA, Porter BA, Olds MO, et al. MR imaging of hemorrhagic adnexal masses. JCAT 1987;11:664-669.
39. Ja S. Perforating hemorrhagic (chocolate) cysts of the ovary; Their importance and specially their relation to pelvic adenomas of the endometrorial type. Arch Surg 1921;3:245-323.
40. Choudhary S, Fasih N, Papadatos D, et al. Unusual imaging appearances of endometriosis. AJR 2009;192:1632-1644.
41. Saba L, Sulcis R, Melis GB, et al. Endometriosis: the role of magnetic resonance imaging. Acta Radiol 2015;56:355-367.
42. Del Frate C, Girometti R, Pittino M, et al. Deep retroperitoneal pelvic endometriosis: MR imaging appearance with laparoscopic correlation. Radiographics 2006;26:1705-1718.
43. Iwamoto H, Suzuki M, Watanabe N, et al. Case study of a pregnant woman with decidualized ovarian endometriosis whose preoperative findings suggested malignant transformation. Eur J Gynaecol Oncol 2006;27:301-303.
44. Sammour RN, Leibovitz Z, Shapiro I, et al. Decidualization of ovarian endometriosis during pregnancy mimicking malignancy. J Ultrasound Med 2005;24:1289-1294.
45. Machida S, Matsubara S, Ohwada M, et al. Decidualization of ovarian endometriosis during pregnancy mimicking malignancy: report of three cases with a literature review. Gynecol Obstet Invest 2008;66:241-247.
46. Miyakoshi K, Tanaka M, Gabionza D, et al. Decidualized ovarian endometriosis mimicking malignancy. AJR 1998;171:1625-1626.
47. Yoshida S, Onogi A, Shigetomi H, et al. Two cases of pregnant women with ovarian endometrioma mimicking a malignant ovarian tumor. J Clin Ultrasound 2008;36:512-516.
48. Barbieri M, Somigliana E, Oneda S, et al. Decidualized ovarian endometriosis in pregnancy: a challenging diagnostic entity. Hum Reprod 2009;24:1818-1824.
49. Takeuchi M, Matsuzaki K, Nishitani H. Magnetic resonance manifestations of decidualized endometriomas during pregnancy. J Comput Assist Tomogr 2008;32:353-355.
50. Stringfellow JM, Hawnaur JM. CT and MRI appearances of sarcomatous change in chronic pelvic endometriosis. Brit J Radiol 1998;71:90-93.
51. Song L, Xing A, Li Q, Wang G. High-Grade Serous Carcinoma Resulting From Rectal Endometriosis and Complicated With Ovarian Cancer. Front Oncol 2019;9.
52. Matsubara S, Kawahara N, Horie A, et al. Magnetic resonance relaxometry improves the accuracy of conventional MRI in the diagnosis of endometriosis-associated ovarian cancer: A case report. Mol Clin Oncol 2019;11:296-300.
| Files | ||
| Issue | Vol 15 No 4 (2023) | |
| Section | Reviews | |
| Keywords | ||
| Endometriosis magnetic resonance imaging (MRI) malignancy mural nodules | ||
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How to Cite
1.
Moradi B, Gity M, Hassani S, Azami M, Rahmani M, Azizi Nik F, Khameneh Bagheri A, Yaghoobpoor S, Ghorani H. MRI Features of Malignant Transformation of Pelvic Endometriosis: A Systematic Review. Basic Clin Cancer Res. 2025;15(4):245-258.
