539550
research-article2014
IJSXXX10.1177/1066896914539550International Journal of Surgical PathologyTorres et al
Case Report
Clear Cell Adenocarcinoma Arising in an Adenomyoma of the Broad Ligament
International Journal of Surgical Pathology 2015, Vol. 23(2) 140–143 © The Author(s) 2014 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/1066896914539550 ijs.sagepub.com
Diogo Torres, MD1, Lynn Parker, MD1, Mana Moghadamfalahi, MD1, Mary Ann Sanders, MD, PhD1, and Daniel S. Metzinger, MD1
Abstract Extrauterine adenomyomas are extremely rare benign tumors of smooth muscles, endometrial glands, and endometrial stroma. Ectopic endometrial glands can undergo malignant change. The ovary is the most common site of malignant change in endometriosis. Cancer arising in extraovarian endometriosis is a rare event with limited cases in the literature. To the best of our knowledge, we present the first case of a clear cell adenocarcinoma arising from foci of ectopic endometrial tissue in an adenomyoma of the broad ligament. It supports the association between endometriomas and clear cell adenocarcinoma. Therefore, patients with a significant history of endometriosis may benefit from close followup or definitive surgery. Keywords ovarian cancer, clear cell adenocarcinoma, clear cell carcinoma, adenomyoma, extraovarian endometriosis, broad ligament
Introduction Endometriosis is defined as the presence of endometrial glands and stroma in extrauterine sites.1 An ademomyoma is distinguished by the presence of specialized endometrioid stroma and smooth muscle within a focus of endometriosis implants.2 Ectopic endometrial tissue may undergo cyclical histologic changes secondary to hormonal influences. Malignant changes were first described by Sampson3 in 1925; today, malignancy arising in endometriosis is a well-established event.4 The ovary is the most common site of malignant change in endometriosis. Although rare, extraovarian cases have been reported in the pelvis and distant sites: the rectovaginal septum, vagina, bladder, pelvic ligaments, umbilicus, cervix, fallopian tube, and abdominal wall. The most common histologic subtype is endometrioid carcinoma.2 Clear cell carcinoma constitutes only a limited number of the cases in the literature.5-8 A set of 3 criteria is used to confirm the endometriotic origin of a malignant neoplasm: (a) the endometriosis is intimately associated with the neoplasm, (b) the histologic type of the neoplasm is compatible with endometrial origin, and (c) no other primary site is identified.4 Adenomyomas are benign intrauterine and extrauterine tumors. They differ from leiomyomas by the presence of intrinisic endometrial glandular and stromal tissues and from entrapped endometrial tissue by the absence of
adhesions, intrauterine adenomyosis, and serial sectioning with no evidence of adjacent endometriosis.2,9,10 Extrauterine adenomyomas are extremely rare; only a few case reports are cited in the literature, none of which gave rise to a malignancy.2,9,10 In this article, we present a case of clear cell carcinoma arising from an adenomyoma associated with foci of endometriosis of the right broad ligament.
Case Presentation A 58-year-old nulligravid female presented to her gynecologist with a chief complaint of postmenopausal bleeding. The patient had not sought medical care in 2 years. She complained of occasional vaginal bleeding for 2 months with acute worsening. Abdomen, adnexa, and uterus were difficult to assess secondary to body habitus. No cervical lesions or discharge was noted. An endometrial biopsy revealed blood and scant fragments of inactive endometrium with fibrin thrombi and stromal breakdown. 1
University of Louisville, Louisville, KY, USA
Corresponding Author: Diogo Torres, Department of Obstetrics, Gynecology & Women’s Health, University of Louisville, 550 South Jackson Street, ACB 2nd Floor, Louisville, KY 40202, USA. Email: [email protected]
141
Torres et al
Figure 1. Gross picture of the specimen with the mass of the right board ligament. The tumor on the right broad ligament is labeled with a black arrow. The right ovary is labeled with a white arrow.
A transvaginal ultrasound revealed an 8.30 × 4.87 × 5.36 cm sized anteverted uterus with an 18-mm endometrial stripe. A 2.28 × 1.49 cm cyst with a 1.26 × 0.98 cm solid area in a 3.20 × 2.32 × 2.40 cm right ovary was noted (Figure 1). The left ovary could not be visualized. CA-125 was 49. On completion of this workup, she was referred to our institution’s Gynecological Oncology Division. Computed tomography scan of the abdomen and pelvis with contrast revealed a 2.8 × 2.9 × 2.8 cm cystic mass in the right adnexa that contained a 10 mm enhancing mural nodule. Several retroperitoneal lymph nodes were identified; the largest aortocaval node measured 7 mm. A left external iliac node measured 11 mm. Concern for malignancy was expressed to the patient and she agreed to proceed with surgery. The patient was taken back to the operating room and the abdomen explored. Pelvic washings were performed and sent to pathology. A 3 cm mass adherent to the serosa of the uterus was visualized; it appeared to be separate from the right ovary. Bilateral fallopian tubes and ovaries were visibly normal. The uterus otherwise appeared normal. On further exploration, there was no evidence of metastasis or extensive disease. The decision was made to proceed with a total robotic hysterectomy and bilateral salpingo-oophorectomy. Frozen section was consistent with clear cell carcinoma. Therefore, staging was performed. Peritoneal biopsies were taken of the bilateral pelvis, anterior bladder peritoneum, posterior cul-de-sac, bilateral colic gutters, and diaphragm. Furthermore, an infracolic omentectomy and bilateral pelvic lymph node dissection was performed. Secondary to body habitus and bowel, the paraortic area
Figure 2. Microscopic picture of the background foci of the endometriosis (magnification 10×).
Figure 3. Clear cell carcinoma, tubulocystic pattern, and hobnailing of the nuclei (magnification 40×).
could not be visualized and sampled. Postoperative course was uncomplicated. Final pathology was consistent with a high-grade clear cell adenocarcinoma intactly located in the right broad ligament adjacent to the proximal portion of the right fallopian tube and attached to the serosa of the uterus, arising from in an adenomyoma (Figures 2 and 3) . The focus of the adenocarcinoma measured 2.0 cm and the adenomyoma measured 4.0 cm in greatest dimension. Additionally, foci of endometriosis involving the serosa of the left ovary and right broad ligament were identified. Some foci of endometriosis showed nuclear atypia. The cancer was reported to arise from the focus of endometriosis in the adenomyoma. All other specimens were negative for metastatic carcinoma.
142 On follow-up at the Gynecologic Oncology Clinic, the final pathology was discussed with the patient, and the decision was made to proceed with weekly dose of dense paclitaxel/carboplatin adjuvant chemotherapy.
Discussion Clear cell tumors are uncommon. Common presentations include abnormal uterine bleeding and abdominal pain in a nulliparous, perimenopsausal woman, as was present in our patient.6,11,12 Although most frequent in the ovary, clear cell carcinomas can also arise in the endometrium and vagina. Grossly, they resemble endometrioid tumors. Histologically, they are defined by distinctive clearing of the cytoplasm; the neoplastic cells can grow in any combination of solid, glandular, tubulocystic, or papillary configurations.13 Half the cases of clear cell carcinoma are associated with endometriosis. Sampson’s criterion is used to confirm the endometriotic origin of a malignancy.3 Our tumor met all 3 of Sampson’s criteria for development of carcinoma in endometriosis. Clear cell histology in ovarian endometriosis is well established8; however, it is especially rare in extraovarian sites. There are fewer than 60 reported cases in the literature.5 Clear cell carcinoma is thought to represent only 5% of these malignancies; most are of endometrioid histology (88%).14 Cells can grow in any combination of solid, glandular, tubulocystic, or papillary configurations. Clear cell carcinomas are biologically aggressive neoplasms with suggestive adverse prognostic indicators: young age, advanced stage, increased mitotic rate, and vascular invasion.13 Conversely, the presence of predominantly (>75%) papillary or tubulocystic morphology may be a favorable prognostic factor.10,13 In a recent case series, the only case (1 of 6) with no evidence of disease for more than 3 years had a pure tubulocystic pattern.14 Our tumor had more than 90% histological evidence of this seemingly favorable architectural pattern of growth. Furthermore, clear cell carcinomas arising in extraovarian endometriosis behave differently than endometrioid carcinomas arising in extraovarian endometriosis and clear cell carcinomas of different origin.14 In the present series of clear cell carcinomas, only 1 case (16% of the total 6) did not have evidence of disease at 3-year follow-up. Conversely, more than 75% of endometrioid carcinomas arising in extragonodal endometriosis with an available statement on survival did not reccur.6 Although 5 of the 6 tumors measured 6 cm or more, prognosis appears impartial to size. A 1.5-cm vaginal tumor metastasized to the inguinal and supraclavicular lymph nodes 9 months after radical surgery.6,14-16 Hence, it appears that in extraovarian endometriosis, clear cell carcinoma has a worse prognosis than endometrioid carcinoma. Our patient’s tumor measured 2.0 cm in greatest
International Journal of Surgical Pathology 23(2) dimension. No evidence of recurrence has been noted at follow-up. Adenoyomas are characterized by endometrial glands and stroma randomly distributed in benign anastamosing fascicles of smooth muscle cells in the absence of a distinct central cavity. They are usually benign intrauterine tumors; extrauterine adenomyomas are a rare entity. Reported cases vary in symptomology, demographics, and location.2,9,10,17 The age of our patient and size of the tumor are within the reported range; however, in our case, the adenomyoma was located in the broad ligament and associated with a clear cell adenocarcinoma. Our case report seems to suggest that foci of endometrial glands within the adenomyoma are capable of transforming into a malignancy. Recent literature indicates that clear cell and low-grade endometrioid carcinoma develop from endometriosis; our case supports this observation.1,18-20 The possible pathogenesis of clear cell carcinoma from foci of endometriosis brings to the forefront the potential clinical implications of this theory.1,18-20 Patients with findings of significant endometriosis may be at higher risk of clear cell and endometrioid adenocarcinoma and should be followed carefully. Because most of these tumors are diagnosed at advanced stage, these patients may also benefit from definitive surgery, including hysterectomy, bilateral salpingo-oophorectomy, and resection of endometriosis on completion of childbearing. Further investigation in this patient population is needed. The effect of specialized endometrioid stroma and smooth muscle on the growth and transformation of endometriosis is unknown. Follow-up of our patient may offer insight on the behavior of adenomyomas and whether clear cell carcinomas arising from an adenomyoma behave differently than clear cell carcinomas of different origin. Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding The author(s) received no financial support for the research, authorship, and/or publication of this article.
References 1. Bulun SE. Endometriosis. N Engl J Med. 2009;360:268-279. 2. Sisodia SM, Khan WA, Goel A. Ovarian ligament adenomyoma: report of a rare entity with review of the literature. J Obstet Gynaecol Res. 2012;38:724-728. 3. Sampson JA. Endometrial carcinoma of the ovary arising in endometrial tissue in that origin., Arch Surg. 1925;10(10):172. 4. Montag AG, Jenison EL, Griffiths CT, Welch WR, Lavin PT, Knapp RC. Ovarian clear cell carcinoma. A
Torres et al clinicopathologic analysis of 44 cases. Int J Gynecol Pathol. 1989;8:85-96. 5. Brunson GL, Barclay DL, Sanders M, Araoz CA. Malignant extraovarian endometriosis: two case reports and review of the literature. Gynecol Oncol. 1988;30:123-130. 6. Brooks JJ, Wheeler JE. Malignancy arising in extragonadal endometriosis: a case report and summary of the world literature. Cancer. 1977;40:3065-3073. 7. Greene JW Jr. Carcinoma arising in adenomyosis associated with a feminizing mesenchymoma of the broad ligament. A case report. Am J Obstet Gynecol. 1961;81:272-276. 8. LaGrenade A, Silverberg SG. Ovarian tumors associated with atypical endometriosis. Hum Pathol. 1988;19:10801084. 9. Choudhrie L, Mahajan NN, Solomon MV, Thomas A, Kale AJ, Mahajan K. Ovarian ligament adenomyoma: a case report. Acta Chir Belg. 2007;107:84-85. 10. Moghadamfalahi M, Metzinger DS. Multiple extrauterine adenomyomas presenting in upper abdomen and pelvis: a case report and brief review of the literature. Case Rep Obstet Gynecol. 2012;2012:565901. 11. Czernobilsky B, Silverman BB, Enterline HT. Clear-cell carcinoma of the ovary. A clinicopathologic analysis of pure and mixed forms and comparison with endometrioid carcinoma. Cancer. 1970;25:762-772. 12. Czernobilsky B, Silverman BB, Mikuta JJ. Endometrioid carcinoma of the ovary. A clinicopathologic study of 75 cases. Cancer. 1970;26:1141-1152. 13. Kennedy AW, Biscotti CV, Hart WR, Tuason LJ. Histologic correlates of progression-free interval and survival in
143 ovarian clear cell adenocarcinoma. Gynecol Oncol. 1993;50:334-338. 14. Hitti IF, Glasberg SS, Lubicz S. Clear cell carcinoma arising in extraovarian endometriosis: report of three cases and review of the literature. Gynecol Oncol. 1990;39:314320. 15. Goldberg MI, Belinson JL, Hutson ED, Nordqvist SR. Clear cell adenocarcinoma arising in endometriosis of the rectovaginal septum. Obstet Gynecol. 1978;51(1 suppl):38s-40s. 16. Mesko JD, Gates H, McDonald TW, Youmans R, Lewis J. Clear cell (“mesonephroid”) adenocarcinoma of the vulva arising in endometriosis: a case report. Gynecol Oncol. 1988;29:385-391. 17. Stewart CJ, Leung YC, Mathew R, McCartney AL. Extrauterine adenomyoma with atypical (symplastic) smooth muscle cells: a report of 2 cases. Int J Gynecol Pathol. 2009;28:23-28. 18. Kurman RJ, Shih Ie M. The origin and pathogenesis of epithelial ovarian cancer: a proposed unifying theory. Am J Surg Pathol. 2010;34:433-443. 19. Rosenblatt K, Thomas D. Association between tubal ligation and endometrial cancer. Int J Cancer. 1997;71:129-130. 20. Veras E, Mao TL, Ayhan A, et al. Cystic and adenofibromatous clear cell carcinomas of the ovary: distinctive tumors that differ in their pathogenesis and behavior: a clinicopathologic analysis of 122 cases. Am J Surg Pathol. 2009;33:844853. 21. Winkelman J, Robinson R. Adenocarcinoma of endometrium involving adenomyosis. Report of an unusual case and review of the literature. Cancer. 1966;19:901-908.
Copyright of International Journal of Surgical Pathology is the property of Sage Publications Inc. and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
research-article2014
IJSXXX10.1177/1066896914539550International Journal of Surgical PathologyTorres et al
Case Report
Clear Cell Adenocarcinoma Arising in an Adenomyoma of the Broad Ligament
International Journal of Surgical Pathology 2015, Vol. 23(2) 140–143 © The Author(s) 2014 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/1066896914539550 ijs.sagepub.com
Diogo Torres, MD1, Lynn Parker, MD1, Mana Moghadamfalahi, MD1, Mary Ann Sanders, MD, PhD1, and Daniel S. Metzinger, MD1
Abstract Extrauterine adenomyomas are extremely rare benign tumors of smooth muscles, endometrial glands, and endometrial stroma. Ectopic endometrial glands can undergo malignant change. The ovary is the most common site of malignant change in endometriosis. Cancer arising in extraovarian endometriosis is a rare event with limited cases in the literature. To the best of our knowledge, we present the first case of a clear cell adenocarcinoma arising from foci of ectopic endometrial tissue in an adenomyoma of the broad ligament. It supports the association between endometriomas and clear cell adenocarcinoma. Therefore, patients with a significant history of endometriosis may benefit from close followup or definitive surgery. Keywords ovarian cancer, clear cell adenocarcinoma, clear cell carcinoma, adenomyoma, extraovarian endometriosis, broad ligament
Introduction Endometriosis is defined as the presence of endometrial glands and stroma in extrauterine sites.1 An ademomyoma is distinguished by the presence of specialized endometrioid stroma and smooth muscle within a focus of endometriosis implants.2 Ectopic endometrial tissue may undergo cyclical histologic changes secondary to hormonal influences. Malignant changes were first described by Sampson3 in 1925; today, malignancy arising in endometriosis is a well-established event.4 The ovary is the most common site of malignant change in endometriosis. Although rare, extraovarian cases have been reported in the pelvis and distant sites: the rectovaginal septum, vagina, bladder, pelvic ligaments, umbilicus, cervix, fallopian tube, and abdominal wall. The most common histologic subtype is endometrioid carcinoma.2 Clear cell carcinoma constitutes only a limited number of the cases in the literature.5-8 A set of 3 criteria is used to confirm the endometriotic origin of a malignant neoplasm: (a) the endometriosis is intimately associated with the neoplasm, (b) the histologic type of the neoplasm is compatible with endometrial origin, and (c) no other primary site is identified.4 Adenomyomas are benign intrauterine and extrauterine tumors. They differ from leiomyomas by the presence of intrinisic endometrial glandular and stromal tissues and from entrapped endometrial tissue by the absence of
adhesions, intrauterine adenomyosis, and serial sectioning with no evidence of adjacent endometriosis.2,9,10 Extrauterine adenomyomas are extremely rare; only a few case reports are cited in the literature, none of which gave rise to a malignancy.2,9,10 In this article, we present a case of clear cell carcinoma arising from an adenomyoma associated with foci of endometriosis of the right broad ligament.
Case Presentation A 58-year-old nulligravid female presented to her gynecologist with a chief complaint of postmenopausal bleeding. The patient had not sought medical care in 2 years. She complained of occasional vaginal bleeding for 2 months with acute worsening. Abdomen, adnexa, and uterus were difficult to assess secondary to body habitus. No cervical lesions or discharge was noted. An endometrial biopsy revealed blood and scant fragments of inactive endometrium with fibrin thrombi and stromal breakdown. 1
University of Louisville, Louisville, KY, USA
Corresponding Author: Diogo Torres, Department of Obstetrics, Gynecology & Women’s Health, University of Louisville, 550 South Jackson Street, ACB 2nd Floor, Louisville, KY 40202, USA. Email: [email protected]
141
Torres et al
Figure 1. Gross picture of the specimen with the mass of the right board ligament. The tumor on the right broad ligament is labeled with a black arrow. The right ovary is labeled with a white arrow.
A transvaginal ultrasound revealed an 8.30 × 4.87 × 5.36 cm sized anteverted uterus with an 18-mm endometrial stripe. A 2.28 × 1.49 cm cyst with a 1.26 × 0.98 cm solid area in a 3.20 × 2.32 × 2.40 cm right ovary was noted (Figure 1). The left ovary could not be visualized. CA-125 was 49. On completion of this workup, she was referred to our institution’s Gynecological Oncology Division. Computed tomography scan of the abdomen and pelvis with contrast revealed a 2.8 × 2.9 × 2.8 cm cystic mass in the right adnexa that contained a 10 mm enhancing mural nodule. Several retroperitoneal lymph nodes were identified; the largest aortocaval node measured 7 mm. A left external iliac node measured 11 mm. Concern for malignancy was expressed to the patient and she agreed to proceed with surgery. The patient was taken back to the operating room and the abdomen explored. Pelvic washings were performed and sent to pathology. A 3 cm mass adherent to the serosa of the uterus was visualized; it appeared to be separate from the right ovary. Bilateral fallopian tubes and ovaries were visibly normal. The uterus otherwise appeared normal. On further exploration, there was no evidence of metastasis or extensive disease. The decision was made to proceed with a total robotic hysterectomy and bilateral salpingo-oophorectomy. Frozen section was consistent with clear cell carcinoma. Therefore, staging was performed. Peritoneal biopsies were taken of the bilateral pelvis, anterior bladder peritoneum, posterior cul-de-sac, bilateral colic gutters, and diaphragm. Furthermore, an infracolic omentectomy and bilateral pelvic lymph node dissection was performed. Secondary to body habitus and bowel, the paraortic area
Figure 2. Microscopic picture of the background foci of the endometriosis (magnification 10×).
Figure 3. Clear cell carcinoma, tubulocystic pattern, and hobnailing of the nuclei (magnification 40×).
could not be visualized and sampled. Postoperative course was uncomplicated. Final pathology was consistent with a high-grade clear cell adenocarcinoma intactly located in the right broad ligament adjacent to the proximal portion of the right fallopian tube and attached to the serosa of the uterus, arising from in an adenomyoma (Figures 2 and 3) . The focus of the adenocarcinoma measured 2.0 cm and the adenomyoma measured 4.0 cm in greatest dimension. Additionally, foci of endometriosis involving the serosa of the left ovary and right broad ligament were identified. Some foci of endometriosis showed nuclear atypia. The cancer was reported to arise from the focus of endometriosis in the adenomyoma. All other specimens were negative for metastatic carcinoma.
142 On follow-up at the Gynecologic Oncology Clinic, the final pathology was discussed with the patient, and the decision was made to proceed with weekly dose of dense paclitaxel/carboplatin adjuvant chemotherapy.
Discussion Clear cell tumors are uncommon. Common presentations include abnormal uterine bleeding and abdominal pain in a nulliparous, perimenopsausal woman, as was present in our patient.6,11,12 Although most frequent in the ovary, clear cell carcinomas can also arise in the endometrium and vagina. Grossly, they resemble endometrioid tumors. Histologically, they are defined by distinctive clearing of the cytoplasm; the neoplastic cells can grow in any combination of solid, glandular, tubulocystic, or papillary configurations.13 Half the cases of clear cell carcinoma are associated with endometriosis. Sampson’s criterion is used to confirm the endometriotic origin of a malignancy.3 Our tumor met all 3 of Sampson’s criteria for development of carcinoma in endometriosis. Clear cell histology in ovarian endometriosis is well established8; however, it is especially rare in extraovarian sites. There are fewer than 60 reported cases in the literature.5 Clear cell carcinoma is thought to represent only 5% of these malignancies; most are of endometrioid histology (88%).14 Cells can grow in any combination of solid, glandular, tubulocystic, or papillary configurations. Clear cell carcinomas are biologically aggressive neoplasms with suggestive adverse prognostic indicators: young age, advanced stage, increased mitotic rate, and vascular invasion.13 Conversely, the presence of predominantly (>75%) papillary or tubulocystic morphology may be a favorable prognostic factor.10,13 In a recent case series, the only case (1 of 6) with no evidence of disease for more than 3 years had a pure tubulocystic pattern.14 Our tumor had more than 90% histological evidence of this seemingly favorable architectural pattern of growth. Furthermore, clear cell carcinomas arising in extraovarian endometriosis behave differently than endometrioid carcinomas arising in extraovarian endometriosis and clear cell carcinomas of different origin.14 In the present series of clear cell carcinomas, only 1 case (16% of the total 6) did not have evidence of disease at 3-year follow-up. Conversely, more than 75% of endometrioid carcinomas arising in extragonodal endometriosis with an available statement on survival did not reccur.6 Although 5 of the 6 tumors measured 6 cm or more, prognosis appears impartial to size. A 1.5-cm vaginal tumor metastasized to the inguinal and supraclavicular lymph nodes 9 months after radical surgery.6,14-16 Hence, it appears that in extraovarian endometriosis, clear cell carcinoma has a worse prognosis than endometrioid carcinoma. Our patient’s tumor measured 2.0 cm in greatest
International Journal of Surgical Pathology 23(2) dimension. No evidence of recurrence has been noted at follow-up. Adenoyomas are characterized by endometrial glands and stroma randomly distributed in benign anastamosing fascicles of smooth muscle cells in the absence of a distinct central cavity. They are usually benign intrauterine tumors; extrauterine adenomyomas are a rare entity. Reported cases vary in symptomology, demographics, and location.2,9,10,17 The age of our patient and size of the tumor are within the reported range; however, in our case, the adenomyoma was located in the broad ligament and associated with a clear cell adenocarcinoma. Our case report seems to suggest that foci of endometrial glands within the adenomyoma are capable of transforming into a malignancy. Recent literature indicates that clear cell and low-grade endometrioid carcinoma develop from endometriosis; our case supports this observation.1,18-20 The possible pathogenesis of clear cell carcinoma from foci of endometriosis brings to the forefront the potential clinical implications of this theory.1,18-20 Patients with findings of significant endometriosis may be at higher risk of clear cell and endometrioid adenocarcinoma and should be followed carefully. Because most of these tumors are diagnosed at advanced stage, these patients may also benefit from definitive surgery, including hysterectomy, bilateral salpingo-oophorectomy, and resection of endometriosis on completion of childbearing. Further investigation in this patient population is needed. The effect of specialized endometrioid stroma and smooth muscle on the growth and transformation of endometriosis is unknown. Follow-up of our patient may offer insight on the behavior of adenomyomas and whether clear cell carcinomas arising from an adenomyoma behave differently than clear cell carcinomas of different origin. Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding The author(s) received no financial support for the research, authorship, and/or publication of this article.
References 1. Bulun SE. Endometriosis. N Engl J Med. 2009;360:268-279. 2. Sisodia SM, Khan WA, Goel A. Ovarian ligament adenomyoma: report of a rare entity with review of the literature. J Obstet Gynaecol Res. 2012;38:724-728. 3. Sampson JA. Endometrial carcinoma of the ovary arising in endometrial tissue in that origin., Arch Surg. 1925;10(10):172. 4. Montag AG, Jenison EL, Griffiths CT, Welch WR, Lavin PT, Knapp RC. Ovarian clear cell carcinoma. A
Torres et al clinicopathologic analysis of 44 cases. Int J Gynecol Pathol. 1989;8:85-96. 5. Brunson GL, Barclay DL, Sanders M, Araoz CA. Malignant extraovarian endometriosis: two case reports and review of the literature. Gynecol Oncol. 1988;30:123-130. 6. Brooks JJ, Wheeler JE. Malignancy arising in extragonadal endometriosis: a case report and summary of the world literature. Cancer. 1977;40:3065-3073. 7. Greene JW Jr. Carcinoma arising in adenomyosis associated with a feminizing mesenchymoma of the broad ligament. A case report. Am J Obstet Gynecol. 1961;81:272-276. 8. LaGrenade A, Silverberg SG. Ovarian tumors associated with atypical endometriosis. Hum Pathol. 1988;19:10801084. 9. Choudhrie L, Mahajan NN, Solomon MV, Thomas A, Kale AJ, Mahajan K. Ovarian ligament adenomyoma: a case report. Acta Chir Belg. 2007;107:84-85. 10. Moghadamfalahi M, Metzinger DS. Multiple extrauterine adenomyomas presenting in upper abdomen and pelvis: a case report and brief review of the literature. Case Rep Obstet Gynecol. 2012;2012:565901. 11. Czernobilsky B, Silverman BB, Enterline HT. Clear-cell carcinoma of the ovary. A clinicopathologic analysis of pure and mixed forms and comparison with endometrioid carcinoma. Cancer. 1970;25:762-772. 12. Czernobilsky B, Silverman BB, Mikuta JJ. Endometrioid carcinoma of the ovary. A clinicopathologic study of 75 cases. Cancer. 1970;26:1141-1152. 13. Kennedy AW, Biscotti CV, Hart WR, Tuason LJ. Histologic correlates of progression-free interval and survival in
143 ovarian clear cell adenocarcinoma. Gynecol Oncol. 1993;50:334-338. 14. Hitti IF, Glasberg SS, Lubicz S. Clear cell carcinoma arising in extraovarian endometriosis: report of three cases and review of the literature. Gynecol Oncol. 1990;39:314320. 15. Goldberg MI, Belinson JL, Hutson ED, Nordqvist SR. Clear cell adenocarcinoma arising in endometriosis of the rectovaginal septum. Obstet Gynecol. 1978;51(1 suppl):38s-40s. 16. Mesko JD, Gates H, McDonald TW, Youmans R, Lewis J. Clear cell (“mesonephroid”) adenocarcinoma of the vulva arising in endometriosis: a case report. Gynecol Oncol. 1988;29:385-391. 17. Stewart CJ, Leung YC, Mathew R, McCartney AL. Extrauterine adenomyoma with atypical (symplastic) smooth muscle cells: a report of 2 cases. Int J Gynecol Pathol. 2009;28:23-28. 18. Kurman RJ, Shih Ie M. The origin and pathogenesis of epithelial ovarian cancer: a proposed unifying theory. Am J Surg Pathol. 2010;34:433-443. 19. Rosenblatt K, Thomas D. Association between tubal ligation and endometrial cancer. Int J Cancer. 1997;71:129-130. 20. Veras E, Mao TL, Ayhan A, et al. Cystic and adenofibromatous clear cell carcinomas of the ovary: distinctive tumors that differ in their pathogenesis and behavior: a clinicopathologic analysis of 122 cases. Am J Surg Pathol. 2009;33:844853. 21. Winkelman J, Robinson R. Adenocarcinoma of endometrium involving adenomyosis. Report of an unusual case and review of the literature. Cancer. 1966;19:901-908.
Copyright of International Journal of Surgical Pathology is the property of Sage Publications Inc. and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
