Uterine Metastasis from Carcinoma of Breast – A Systematic Analysis

• Sajad Ahmad Salati

  Department of Surgery, Unaizah College of Medicine and Medical Sciences, Qassim University, Kingdom of Saudi Arabia

• Mohammed Alfehaid

  Department of Surgery, Unaizah College of Medicine and Medical Sciences, Qassim University, Kingdom of Saudi Arabia

• Lamees Sulaiman Alsulaim

  Department of Surgery, Unaizah College of Medicine and Medical Sciences, Qassim University, Kingdom of Saudi Arabia

• Saleh Ahmad Alsuwaydani

  Department of Surgery, Unaizah College of Medicine and Medical Sciences, Qassim University, Kingdom of Saudi Arabia

• Mohammed Ahmed Elmuttalut

  Department of Community Medicine, Al-Rayan College of Medicine, Al-MadinaAl-Munawwarrah, Kingdom of Saudi Arabia

Breast cancer can metastasize to a wide range of organs, but reports about uterine metastases are rare. The current article systematically analyzes 55 patients reported in peer-reviewed literature from 2010–2022 with respect to nine variables, including: [i] age of the patient; [ii] clinical presentation of uterine metastasis; [iii] precise location of metastasis; [iv] primary (breast) cancer histopathology; [v] imaging modality utilized for detection of metastasis; [vi] timing of appearance of metastases: synchronous or metachronous; [vii] immunochemistry markers; [viii] management; and [ix] survival. Uterine metastases may appear in synchronous or metachronous fashion and may be asymptomatic or have symptoms like abnormal vaginal bleeding. Treatment of uterine metastases usually comprises of total abdominal hysterectomy with bilateral salpingo-oophorectomy along with chemotherapy. The long-term prognosis is unclear, but due to the development of metastases in other bodily parts, cases frequently have a poor outcome.

Di Micco R, Santurro L, Gasparri ML, Zuber V, Fiacco E, Gazzetta G, Smart CE, Valentini A, Gentilini OD. Rare sites of breast cancer metastasis: a review. Transl Cancer Res 2019; 8(Suppl 5): S518-S552. https://doi.org/10.21037/tcr.2019.07.24

Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018; 68(6): 394-424. https://doi.org/10.3322/caac.21492

Runowicz CD, Leach CR, Henry NL, Henry KS, Mackey HT, Cowens-Alvarado RL, Cannady RS, Pratt-Chapman ML, Edge SB, Jacobs LA, Hurria A, Marks LB, LaMonte SJ, Warner E, Lyman GH, Ganz PA. American Cancer Society/American Society of Clinical Oncology Breast Cancer Survivorship Care Guideline. CA Cancer J Clin 2016; 66(1): 43-73. https://doi.org/10.3322/caac.21319

Khatcheressian JL, Hurley P, Bantug E, Esserman LJ, Grunfeld E, Halberg F, Hantel A, Henry NL, Muss HB, Smith TJ, Vogel VG, Wolff AC, Somerfield MR, Davidson NE. American Society of Clinical Oncology. Breast cancer follow-up and management after primary treatment: American Society of Clinical Oncology clinical practice guideline update. J Clin Oncol 2013; 31(7): 961-65. https://doi.org/10.1200/JCO.2012.45.9859

Bogliolo S, Morotti M, ValenzanoMenada M, Fulcheri E, Musizzano Y, Casabona F. Breast cancer with synchronous massive metastasis in the uterine cervix: a case report and review of the literature. Arch Gynecol Obstet 2010; 281(4): 769-73. https://doi.org/10.1007/s00404-009-1264-0

D'souza MM, Sharma R, Tripathi M, Saw SK, Anand A, Singh D, Mondal A. Cervical and uterine metastasis from carcinoma of breast diagnosed by PET/CT: an unusual presentation. ClinNucl Med 2010; 35(10): 820-23. https://doi.org/10.1097/RLU.0b013e3181ef0b1b

Hara F, Kiyoto S, Takabatake D, Takashima S, Aogi K, Ohsumi S, Teramoto N, Nishimura R, Takashima S. Endometrial Metastasis from Breast Cancer during Adjuvant Endocrine Therapy. Case Rep Oncol 2010; 3(2): 137-41. https://doi.org/10.1159/000313921

Hooker AB, Radder CM, van de Wiel B, Geenen MM. Metastasis from breast cancer to an endometrial polyp; treatment options and follow-up. Report of a case and review of the literature. Eur J Gynaecol Oncol 2011; 32(2): 228-30.

Abaid LN, Rhee JM, Rausei-Mills V, Lim J, Police AM, Goldstein BH. Metastatic lobular breast carcinoma infiltrating a uterine leiomyoma. J Minim Invasive Gynecol 2011; 18(5): 674-77. https://doi.org/10.1016/j.jmig.2011.06.008

Dirican A, Kucukzeybek Y, Somali I, Erten C, Demir L, Can A, et al. Micro-metastases into the uterine leiomyoma from invasive ductal breast cancer under adjuvant tamoxifen therapy: case report. Eur J Gynaecol Oncol 2012; 33(6): 652-55.

vanMeurs HS, Dieles JJ, Stel HV. A uterine leiomyoma in which a leiomyosarcoma with osteoclast-like giant cells and a metastasis of a ductal breast carcinoma are present. Ann Diagn Pathol 2012; 16(1): 67-70. https://doi.org/10.1016/j.anndiagpath.2010.11.010

Horikawa M, Mori Y, Nagai S, Tanaka S, Saito S, Okamoto T. Metastatic breast cancer to the uterine cervix mimicking a giant cervical leiomyoma. Nagoya J Med Sci 2012; 74(3-4): 347-51.

Arslan D, Tural D, Tatlı AM, Akar E, Uysal M, Erdoğan G. Isolated uterine metastasis of invasive ductal carcinoma. Case Rep Oncol Med 2013; 2013: 793418. https://doi.org/10.1155/2013/793418

Muñoz-Iglesias J, Uña-Gorospe J, Allende-Riera A, De Sequera-Rahola M, Cárdenas-Negro C. Unsuspected uterine metastasis of breast carcinoma diagnosed by 18F-FDG PET/CT. ClinNucl Med 2013; 38(11): e441-42. https://doi.org/10.1097/RLU.0b013e318292a73b

Alheeti S, Qureshi A, Ansari N, Murphy JF. Metastatic Breast Cancer of the Cervix Presenting in Labor. Bahrain Med Bull 2014; 36(2): 112-13.

Binstock A, Smith AL, Olawaiye AB. Recurrent breast carcinoma presenting as postmenopausal vaginal bleeding: A case report. Gynecol Oncol Rep 2013; 10: 38-40. https://doi.org/10.1016/j.gynor.2013.06.003

Bezpalko K, Mohamed MA, Mercer L, McCann M, Elghawy K, Wilson K. Concomitant endometrial and gallbladder metastasis in advanced multiple metastatic invasive lobular carcinoma of the breast: A rare case report. Int J Surg Case Rep 2015; 14: 141-45. https://doi.org/10.1016/j.ijscr.2015.07.036

Haeri H, Movarrei F, Shaker G. Metastatic breast cancer to uterine leiomyoma: case report. Tehran Univ Med J 2015; 73(5): 391-95.

Huo Z, Gao Y, Zuo W, Zheng G, Kong R. Metastases of basal-like breast invasive ductal carcinoma to the endometrium: A case report and review of the literature. Thorac Cancer 2015; 6(4): 548-52. https://doi.org/10.1111/1759-7714.12195

Pekindil G, Solmaz Hasdemir P, Tan A, Goksel G. Breast Cancer with Silent Metas-tasis to Uterine Cervix. J Clin Anal Med 2015; 6(suppl 5): 647-49

Toyoshima M, Iwahashi H, Shima T, Hayasaka A, Kudo T, Makino H, Igeta S, Matsuura R, Ishigaki N, Akagi K, Sakurada J, Suzuki H, Yoshinaga K. Solitary uterine metastasis of invasive lobular carcinoma after adjuvant endocrine therapy: a case report. J Med Case Rep 2015; 9: 47. https://doi.org/10.1186/s13256-014-0511-6

Lokadasan R, Ratheesan K, Sukumaran R, Nair SP. Metastatic lobular carcinoma of breast mimics primary cervix carcinoma: two case reports and a review of the literature. Ecancermedicalscience 2015; 9: 571. https://doi.org/10.3332/ecancer.2015.571

Waks AG, Lennon J, Yadav BS, Hwang H, dSchapirael Carmen M, Johnson NB, Reynolds K, Schapira L, Gilman PB, Overmoyer B. Metastasis to the Cervix Uteri 15 Years After Treatment of Lobular Carcinoma of the Breast. Semin Oncol 2015; 42(4): e81-94. https://doi.org/10.1053/j.seminoncol.2015.07.002

Razia S, Nakayama K, Tsukao M, Nakamura K, Ishikawa M, Ishibashi T, Ishikawa N, Sanuki K, Yamashita H, Ono R, Hossain MM, Minamoto T, Kyo S. Metastasis of breast cancer to an endometrial polyp, the cervix and a leiomyoma: A case report and review of the literature. Oncol Lett 2017; 14(4): 4585-92. https://doi.org/10.3892/ol.2017.6822

Seo SY, Shin JY, Ji YI. Metastatic uterine cancer looking as cervical fibroid in recurrent breast cancer woman: a case report. ObstetGynecol Sci 2017; 60(5): 481-84. https://doi.org/10.5468/ogs.2017.60.5.481

Hajal E, Dabaj E, Kassem M, Snaifer E, Ghandour F. Endometrial Metastasis from a Breast Carcinoma Simulating a Primary Uterine Malignancy. J Adenocarcinoma 2017; 2: 1. https://doi.org/10.21767/2572-309X.100016

Chupryna E, Ganovska A, Kirilova I, Kovachev S, Baytchev G. Endometrial and cervical metastases leading to the diagnosis of a primary breast cancer: A case report. Int J Surg Med 2017; 3(4): 253-56.

Trihia H, Gavresea T, Novkovic N. Lobular carcinoma metastasis to endometrial polyp 19 years after primary diagnosis: a report of an exceptional case. J Clin Obstet Gynecol Infertil 2017; 1(4): 1019.

Akinpeloye A, Satti M, Congdon D, BoikeG . Breast Cancer Masquerades as an Endometrial Cancer. Obstet Gynecol Cases Rev 2017; 4: 103. https://doi.org/10.23937/2377-9004/1410103

Akhtar A, Ratra A, Puckett Y, Sheikh AB, Ronaghan CA. Synchronous Uterine Metastases from Breast Cancer: Case Study and Literature Review. Cureus 2017; 9(11): e1840. https://doi.org/10.7759/cureus.1840

Abdalla AS, Lazarevska A, Omer MM, Tan E, Asaad A, Sathananthan S. Metastatic Breast Cancer to the Cervix Presenting with Abnormal Vaginal Bleeding During Chemotherapy: A Case Report and Literature Review. Chirurgia (Bucur) 2018; 113(4): 564-70. https://doi.org/10.21614/chirurgia.113.4.564

Berger AA, Matrai CE, Cigler T, Frey MK. Palliative hysterectomy for vaginal bleeding from breast cancer metastatic to the uterus. Ecancermedicalscience 2018; 12: 811. https://doi.org/10.3332/ecancer.2018.811

Briki R, Cherif O, Bannour B, Hidar S, Boughizane S, Khairi H. Uncommon metastases of invasive lobular breast cancer to the endometrium: a report of two cases and review of the literature. Pan Afr Med J 2018; 30: 268. https://doi.org/10.11604/pamj.2018.30.268.16208

Thouvenot A, Bizet Y, Baccar LS, Lamuraglia M. Primary breast cancer relapse as metastasis to the cervix uteri: A case report. Mol Clin Oncol 2018; 9(1): 96-97. https://doi.org/10.3892/mco.2018.1627

Rahmani M, Nili F, Tabibian E. Endometrial Metastasis from Ductal Breast Carcinoma: A Case Report with Literature Review. Am J Case Rep 2018; 19: 494-99. https://doi.org/10.12659/AJCR.907638

Cimpeanu E, Ahmed J, Tricorico G, Bardarov S, Shulimovich M, Lakhi N. Unique presentation of occult breast cancer with uterine cervix metastasis. Clin Case Rep 2019; 7(8): 1573-76. https://doi.org/10.1002/ccr3.2306

Franco-Márquez R, Torres-Gaytán AG, Narro-Martinez MA, Carrasco-Chapa A, Núñez BG, Boland-Rodriguez E. Metastasis of Breast Lobular Carcinoma to Endometrium Presenting as Recurrent Abnormal Uterine Bleeding: A Case Report and Review of Literature. Case Rep Pathol 2019; 2019: 5357194. https://doi.org/10.1155/2019/5357194

Homsi MEl, Barakat A, Rammal R, Haidar M. Uterine metastasis from invasive ductal breast carcinoma mimicking fibroid features on MRI and detected by FDG PET/CT: role of SUVmax. Eur J Gynaecol Oncol 2019; 40(6): 1079-82. https://doi.org/10.12892/ejgo4771.2019

Silva Fontinele DR, Vieira SC, da Silva Júnior RG, Rodrigues TS. Lobular carcinoma of the breast with metastasis to the uterine cervix. J Can Res Ther 2019; 15: 1411-4. https://doi.org/10.4103/jcrt.JCRT_469_18

Arif SH, Mohammed AA, Mohammed FR. Metastatic invasive lobular carcinoma of the breast to the endometrium presenting with abnormal uterine bleeding; Case report. Ann Med Surg (Lond) 2020; 51: 41-43. https://doi.org/10.1016/j.amsu.2020.01.008

Abdallah H, Elwy A, Alsayed A, Rabea A, Magdy N. Metastatic Breast Lobular Carcinoma to Unusual Sites: A Report of Three Cases and Review of Literature. J Med Cases 2020; 11(9): 292-95. https://doi.org/10.14740/jmc3538

Farkas A, Rigney D, Shenoy V, Nutter K. (Nov 06, 2020). Breast Cancer Metastasis to the Endometrium. Appl Radiol 2020; 49(6): 52-53.

Qawasmeh J, A-Hussaini M, Koro S. Invasive Ductal Carcinoma of the Breast with Metastasis to the Uterine Cervix. Clin Case Rep Int 2020; 4: 1172.

Goel S, Sharma PK, Lodha M. A Rare Case of Cervix Metastasis from a Breast Primary. Cancer Ther Oncol Int J 2020; 17(1): CTOIJ.MS.ID.555954. https://doi.org/10.19080/CTOIJ.2020.17.555954

Danolić D, Marcelić L, Alvir I, Mamić I, Sušnjar L, Rendić-miočević Z, Puljiz M. Rare case of invasive lobular breast cancer metastasis to the endometrium. Lib Oncol 2020; 48(2-3): 116-18. https://doi.org/10.20471/LO.2020.48.02-03.19

Gomez M, Whitting K, Naous R. Lobular breast carcinoma metastatic to the endometrium in a patient under tamoxifen therapy: A case report. SAGE Open Med Case Rep 2020; 8: 2050313X20907208. https://doi.org/10.1177/2050313X20907208

Cochrane E, Kim S, Kudelka A, Burke W. Invasive ductal breast carcinoma metastasis to the cervix: A case review and clinical correlation. Gynecol Oncol Rep 2020; 33: 100616. https://doi.org/10.1016/j.gore.2020.100616

Landolfo C, Musone M, Catinella V, Tralongo P, Pozzati F, Quagliozzi L, Bertoldo V, Muratore M, Paris I, Testa AC. A rare case of uterine metastasis from breast cancer. Ultrasound Obstet Gynecol 2021; 58: 100. VP03.04. https://doi.org/10.1002/uog.24048

Awazu Y, Fukuda T, Imai K, Yamauchi M, Kasai M, Ichimura T, Yasui T, Sumi T: Uterine metastasis of lobular breast carcinoma under tamoxifen therapy: A case report. Mol Clin Oncol 2021; 15: 266. https://doi.org/10.3892/mco.2021.2428

Azhar M, Hamdani SAM, Iftikhar J, Ahmad W, Mushtaq S, KalsoomAwan UE. An Unusual Occurrence of Uterine Metastases in a Case of Invasive Ductal Breast Carcinoma. Cureus 2021; 13(11): e19820. https://doi.org/10.7759/cureus.19820

Lim L, Wang TY, Lam HB, Chang CL. Massive metastasis of breast cancer to female genital organs. Taiwan J Obstet Gynecol 2021; 60(3): 563-66. https://doi.org/10.1016/j.tjog.2021.03.033

Varghese MP, Raju S, Savithri MC, Augustine J, Varghese M. Metastatic Breast Carcinoma to The Uterine Cervix - An Unusual Presentation . Annals of Pathology and Laboratory Medicine 2021; 8(2): C32-34. https://doi.org/10.21276/APALM.2944

Dominguez R S, Billod J A. Ovary and Uterus, Rare Sites of Metastases from Breast Cancer: A Case Series. Int J Med Rev Case Rep 2021; 5(6): 79-85. https://doi.org/10.5455/IJMRCR.metastasis-breast-cancer-172-1606462902

Bouvier AS, Panchbhaya N, Brochard C, Marchand E, Mezzadri M, Leveau-Vallier AS, Cornelis F, Benifla JL, Mimoun C. Uterine metastasis from invasive ductal breast carcinoma: A case report with literature review. J Gynecol Obstet Hum Reprod 2021; 50(1): 101993. https://doi.org/10.1016/j.jogoh.2020.101993

Kong D, Dong X, Qin P, Sun D, Zhang Z, Zhang Y, Hao F, Wang M. Asymptomatic uterine metastasis of breast cancer: Case report and literature review. Medicine 2022; 101: 41(e31061). https://doi.org/10.1097/MD.0000000000031061

Subhas N, Patel PV, Pannu HK, Jacene HA, Fishman EK, Wahl RL. Imaging of pelvic malignancies with in-line FDG PET-CT: case examples and common pitfalls of FDG PET. Radiographics 2005; 25(4): 1031-43. https://doi.org/10.1148/rg.254045155

Ma Y, Shao X. Uterine fibroids with positive 18F-FDG PET/CT image and significantly increased CA19-9: A case report. Medicine (Baltimore) 2017; 96(51): e9421. https://doi.org/10.1097/MD.0000000000009421

Zaha DC. Significance of immunohistochemistry in breast cancer. World J Clin Oncol 2014; 5(3): 382-92. https://doi.org/10.5306/wjco.v5.i3.382

Tozbikian GH, Zynger DL. A combination of GATA3 and SOX10 is useful for the diagnosis of metastatic triple-negative breast cancer. Hum Pathol 2019; 85: 221-227. https://doi.org/10.1016/j.humpath.2018.11.005

Han JH, Kang Y, Shin HC, Kim HS, Kang YM, Kim YB, Oh SY. Mammaglobin expression in lymph nodes is an important marker of metastatic breast carcinoma. Arch Pathol Lab Med 2003; 127(10): 1330-4. https://doi.org/10.5858/2003-127-1330-MEILNI

Cummings MC, Simpson PT, Reid LE, Jayanthan J, Skerman J, Song S, McCart Reed AE, Kutasovic JR, Morey AL, Marquart L, O'Rourke P, Lakhani SR. Metastatic progression of breast cancer: insights from 50 years of autopsies. J Pathol 2014; 232(1): 23-31. https://doi.org/10.1002/path.4288

Lamovec J, Bracko M. Metastatic pattern of infiltrating lobular carcinoma of the breast: an autopsy study. J Surg Oncol 1991; 48(1): 28-33. https://doi.org/10.1002/jso.2930480106

Wahed A, Connelly J, Reese T. E-cadherin expression in pleomorphic lobular carcinoma: an aid to differentiation from ductal carcinoma. Ann Diagn Pathol 2002; 6(6): 349-51. https://doi.org/10.1053/adpa.2002.36660

Varga Z, Mallon E. Histology and immunophenotype of invasive lobular breast cancer. daily practice and pitfalls. Breast Dis 2008-2009; 30: 15-9. https://doi.org/10.3233/BD-2009-0278

Kowalski PJ, Rubin MA, Kleer CG. E-cadherin expression in primary carcinomasof the breast and its distant metastases. Breast Cancer Res 2003; 5: R217YR222.

Rodrigues F, Carneiro F, Lopes C. Uterine metastasis from breast cancer – retrospective analysis of 15 cases. Acta Obstet Ginecol Port 2015; 9(1): 27-33.

Karvouni E, Papakonstantinou K, Dimopoulou C, Kairi-Vassilatou E, Hasiakos D, Gennatas CG, Kondi-Paphiti A. Abnormal uterine bleeding as a presentation of metastatic breast disease in a patient with advanced breast cancer. Arch Gynecol Obstet 2009; 279(2): 199-201. https://doi.org/10.1007/s00404-008-0665-9

• PDF

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.