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Clinicopathological characteristics of fallopian tube metastases from primary endometrial, cervical, and nongynecological malignancies: a single institutional experience

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Abstract

This study was aimed at investigating the clinicopathological characteristics of tubal metastases originating from primary endometrial, cervical, and nongynecological malignancies. We performed a 4-year retrospective study in which fallopian tube tissues obtained from 60 patients with tubal metastases were examined. In addition, we compared the number of tubal metastasis cases detected during periods of representative or whole tubal sampling. Twenty-three and 37 tubal metastases were found in cases examined after representative and whole tubal sampling techniques, respectively. Four cases of microscopic tubal metastases were detected via whole sampling, whereas no microscopic lesions were identified via representative sampling. The metastatic lesions originated from 14 uterine (10, endometrium; 4, cervix) and 46 nongynecological tumors (21, colon; 15, stomach; 5, biliary; 3, appendix; 2, breast). Tumors were most commonly involved in the muscle and lamina propria (n = 17). We noted distinctive histopathological features according to the extent of mural involvement: fibromyxoid stromal reaction and lymphohistiocytic infiltration in tumors involving the muscle and subepithelial connective tissue, architectural alterations of plicae in those involving the subepithelial connective tissue, and intraluminal mucinous and inflammatory exudate adjacent to intraepithelial tumors. We observed distinctive histopathological features associated with tubal metastases according to the extent of mural involvement. In addition, we demonstrated that the sampling method used in the routine microscopic examination of the fallopian tube affects the detection of tubal metastases. Our data support the notion that it is more logical to thoroughly sample both the fimbrial ends and the nonfimbriated portions of fallopian tubes for all salpingectomy specimens in the setting of cancer surgery.

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References

  1. Vroomen L, Scheffer HJ, Melenhorst M, van Grieken N, van den Tol MP, Meijerink MR (2017) Irreversible electroporation to treat malignant tumor recurrences within the pelvic cavity: a case series. Cardiovasc Intervent Radiol. doi:10.1007/s00270-017-1657-6

  2. Mazur MT, Hsueh S, Gersell DJ (1984) Metastases to the female genital tract. Analysis of 325 cases. Cancer 53:1978–1984

    Article  CAS  PubMed  Google Scholar 

  3. Charnley RM, Banerjee AK, Whitaker SC, Spiller RC, Doran J (1995) Peritoneal seeding of pancreatic cancer following transperitoneal biliary procedures. Br J Surg 82:393

    Article  CAS  PubMed  Google Scholar 

  4. Finn WF, Javert CT (1949) Primary and metastatic cancer of the fallopian tube. Cancer 2:803–814

    Article  CAS  PubMed  Google Scholar 

  5. Stewart CJ, Leung YC, Whitehouse A (2012) Fallopian tube metastases of non-gynaecological origin: a series of 20 cases emphasizing patterns of involvement including intra-epithelial spread. Histopathology 60:E106–E114. doi:10.1111/j.1365-2559.2012.04194.x

    Article  PubMed  Google Scholar 

  6. Rabban JT, Vohra P, Zaloudek CJ (2015) Nongynecologic metastases to fallopian tube mucosa: a potential mimic of tubal high-grade serous carcinoma and benign tubal mucinous metaplasia or nonmucinous hyperplasia. Am J Surg Pathol 39:35–51. doi:10.1097/PAS.0000000000000293

    Article  PubMed  Google Scholar 

  7. Kurman RJ, Carcangiu ML, Herrington CS, Young RH (2014) World Health Organization classification of tumours of female reproductive organs. International Agency for Research on Cancer. Lyon, France

    Google Scholar 

  8. Bosman FT, Carneiro F, Hruban RH, THeise ND (2010) World Health Organization classification of tumours of the digestive system. International Agency for Research on Cancer, Lyon

  9. Lakhani SR, Ellis IO, Schnitt SJ, Tan PH, van de Vijver MJ (2012) World Health Organization Classification of Tumours International Agency for Research on Cancer, Lyon

  10. Yoon N, Yoon G, Park CK, Kim HS (2016) Stromal p16 expression is significantly increased in malignant ovarian neoplasms. Oncotarget 7:64665–64673. doi:10.18632/oncotarget.11660

    PubMed  PubMed Central  Google Scholar 

  11. Yoon G, Oh CS, Kim HS (2016) Hypergravity upregulates renal inducible nitric oxide synthase expression and nitric oxide production. Oncotarget 7:30147–30154. doi:10.18632/oncotarget.9253

    Article  PubMed  PubMed Central  Google Scholar 

  12. Yoon G, Oh CS, Kim HS (2016) Distinctive expression patterns of hypoxia-inducible factor-1alpha and endothelial nitric oxide synthase following hypergravity exposure. Oncotarget 7:33675–33688. doi:10.18632/oncotarget.9372

    Article  PubMed  PubMed Central  Google Scholar 

  13. Kim HS, Yoon G, Do SI, Kim SJ, Kim YW (2016) Down-regulation of osteoprotegerin expression as a novel biomarker for colorectal carcinoma. Oncotarget 7:15187–15199. doi:10.18632/oncotarget.7885

    Article  PubMed  PubMed Central  Google Scholar 

  14. Yoon G, Won Koh C, Yoon N, Kim JY, Kim HS (2016) Stromal p16 expression is significantly increased in endometrial carcinoma. Oncotarget. doi:10.18632/oncotarget.13594

  15. Park CK, Yoon G, Cho YA, Kim HS (2016) Clinicopathological and immunohistochemical characterization of papillary proliferation of the endometrium: a single institutional experience. Oncotarget 7:39197–39206. doi:10.18632/oncotarget.10049

    Article  PubMed  PubMed Central  Google Scholar 

  16. Jung YY, Nahm JH, Kim HS (2016) Cytomorphological characteristics of glassy cell carcinoma of the uterine cervix: histopathological correlation and human papillomavirus genotyping. Oncotarget 7:74152–74161. doi:10.18632/oncotarget.12361

    PubMed  PubMed Central  Google Scholar 

  17. Kim EK, Yoon G, Kim HS (2016) Chemotherapy-induced endometrial pathology: mimicry of malignancy and viral endometritis. Am J Transl Res 8:2459–2467

    PubMed  PubMed Central  Google Scholar 

  18. Bae GE, Yoon G, Song YJ, Kim HS (2016) High-grade squamous intraepithelial lesion arising adjacent to vulvar lymphangioma circumscriptum: a tertiary institutional experience. Oncotarget 7:48120–48129. doi:10.18632/oncotarget.10158

    Article  PubMed  PubMed Central  Google Scholar 

  19. Soliman PT, Slomovitz BM, Broaddus RR, Sun CC, Oh JC, Eifel PJ, Gershenson DM, Lu KH (2004) Synchronous primary cancers of the endometrium and ovary: a single institution review of 84 cases. Gynecol Oncol 94:456–462. doi:10.1016/j.ygyno.2004.05.006

    Article  PubMed  Google Scholar 

  20. Zhang Y, Garcia-Buitrago MT, Koru-Sengul T, Schuman S, Ganjei-Azar P (2013) An immunohistochemical panel to distinguish ovarian from uterine serous papillary carcinomas. Int J Gynecol Pathol 32:476–481. doi:10.1097/PGP.0b013e31826ddc4e

    Article  CAS  PubMed  Google Scholar 

  21. Elishaev E, Gilks CB, Miller D, Srodon M, Kurman RJ, Ronnett BM (2005) Synchronous and metachronous endocervical and ovarian neoplasms: evidence supporting interpretation of the ovarian neoplasms as metastatic endocervical adenocarcinomas simulating primary ovarian surface epithelial neoplasms. Am J Surg Pathol 29:281–294

    Article  PubMed  Google Scholar 

  22. de Waal YR, Thomas CM, Oei AL, Sweep FC, Massuger LF (2009) Secondary ovarian malignancies: frequency, origin, and characteristics. Int J Gynecol Cancer 19:1160–1165. doi:10.1111/IGC.0b013e3181b33cce

    Article  PubMed  Google Scholar 

  23. Moore RG, Chung M, Granai CO, Gajewski W, Steinhoff MM (2004) Incidence of metastasis to the ovaries from nongenital tract primary tumors. Gynecol Oncol 93:87–91. doi:10.1016/j.ygyno.2003.12.039

    Article  PubMed  Google Scholar 

  24. Ulker V, Numanoglu C, Alpay V, Akbayir O, Polat I, Gedikbasi A, Akca A (2013) Characteristics and prognosis of ovarian metastatic tumors: review of a single-institution experience. Eur J Gynaecol Oncol 34:75–78

    CAS  PubMed  Google Scholar 

  25. Selvaggi LE, Di Vagno G, Loverro G, Masotina A, Cramarossa D, Napoli A, Resta L (1993) Abnormal cervical PAP smear leading to the diagnosis of gastrointestinal cancer without cervico-vaginal metastases. Eur J Gynaecol Oncol 14:398–401

    CAS  PubMed  Google Scholar 

  26. Pambuccian SE, Bachowski GJ, Twiggs LB (2000) Signet ring cell lobular carcinoma of the breast presenting in a cervicovaginal smear. A case report. Acta Cytol 44:824–830

    Article  CAS  PubMed  Google Scholar 

  27. Gemer O, Bergman M, Segal S (2004) Ovarian metastasis in women with clinical stage I endometrial carcinoma. Acta Obstet Gynecol Scand 83:208–210

    Article  PubMed  Google Scholar 

  28. Stewart CJ, Doherty DA, Havlat M, Koay MH, Leung YC, Naran A, O'Brien D, Ruba S, Salfinger S, Tan J (2013) Transtubal spread of endometrial carcinoma: correlation of intra-luminal tumour cells with tumour grade, peritoneal fluid cytology, and extra-uterine metastasis. Pathology 45:382–387. doi:10.1097/PAT.0b013e328360b6e7

    Article  CAS  PubMed  Google Scholar 

  29. Snyder MJ, Bentley R, Robboy SJ (2006) Transtubal spread of serous adenocarcinoma of the endometrium: an underrecognized mechanism of metastasis. Int J Gynecol Pathol 25:155–160. doi:10.1097/01.pgp.0000179614.47838.82

    Article  PubMed  Google Scholar 

  30. Ronnett BM, Yemelyanova AV, Vang R, Gilks CB, Miller D, Gravitt PE, Kurman RJ (2008) Endocervical adenocarcinomas with ovarian metastases: analysis of 29 cases with emphasis on minimally invasive cervical tumors and the ability of the metastases to simulate primary ovarian neoplasms. Am J Surg Pathol 32:1835–1853. doi:10.1097/PAS.0b013e3181758831

    Article  PubMed  Google Scholar 

  31. Sutton GP, Bundy BN, Delgado G, Sevin BU, Creasman WT, Major FJ, Zaino R (1992) Ovarian metastases in stage IB carcinoma of the cervix: a Gynecologic Oncology Group study. Am J Obstet Gynecol 166:50–53

    Article  CAS  PubMed  Google Scholar 

  32. Ngamcherttakul V, Ruengkhachorn I (2012) Ovarian metastasis and other ovarian neoplasms in women with cervical cancer stage IA-IIA. Asian Pac J Cancer Prev 13:4525–4529

    Article  PubMed  Google Scholar 

  33. Shimada M, Kigawa J, Nishimura R, Yamaguchi S, Kuzuya K, Nakanishi T, Suzuki M, Kita T, Iwasaka T, Terakawa N (2006) Ovarian metastasis in carcinoma of the uterine cervix. Gynecol Oncol 101:234–237. doi:10.1016/j.ygyno.2005.10.004

    Article  PubMed  Google Scholar 

  34. Reyes C, Murali R, Park KJ (2015) Secondary involvement of the adnexa and uterine corpus by carcinomas of the uterine cervix: a detailed morphologic description. Int J Gynecol Pathol 34:551–563. doi:10.1097/PGP.0000000000000206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Deel CD, Allen RA, Holman LL, Zuna RE (2016) Adenocarcinoma of the cervix involving the fallopian tube mucosa: report of a case. Diagn Pathol 11:77. doi:10.1186/s13000-016-0529-8

    Article  PubMed  PubMed Central  Google Scholar 

  36. Gungor T, Altinkaya SO, Ozat M, Akbay S, Mollamahmutoglu L (2011) Unusual form of superficial spreading squamous cell carcinoma of cervix involving the endometrium, bilateral tubes and ovaries: a case report with literature review. Arch Gynecol Obstet 283:323–327. doi:10.1007/s00404-010-1672-1

    Article  PubMed  Google Scholar 

  37. Pins MR, Young RH, Crum CP, Leach IH, Scully RE (1997) Cervical squamous cell carcinoma in situ with intraepithelial extension to the upper genital tract and invasion of tubes and ovaries: report of a case with human papilloma virus analysis. Int J Gynecol Pathol 16:272–278

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (2016R1D1A1B03935584) and by a faculty research grant of Yonsei University College of Medicine for 2016 (6-2017-0036).

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  1. Department of Pathology, Severance Hospital, Yonsei University College of Medicine, 50-1, Yonsei-ro, Seodaemun-gu, Seoul, 03722, Republic of Korea

    Kiyong Na & Hyun-Soo Kim

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  1. Kiyong Na
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  2. Hyun-Soo Kim
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Correspondence to Hyun-Soo Kim.

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This study was reviewed and approved by the Institutional Review Board at the Severance Hospital, Yonsei University Health System, Seoul, Republic of Korea (2016-2886-001).

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The authors declare that they have no conflict of interest.

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Na, K., Kim, HS. Clinicopathological characteristics of fallopian tube metastases from primary endometrial, cervical, and nongynecological malignancies: a single institutional experience. Virchows Arch 471, 363–373 (2017). https://doi.org/10.1007/s00428-017-2186-z

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  • DOI: https://doi.org/10.1007/s00428-017-2186-z

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