Abstract
Purpose
This study aimed to analyze the clinicopathological features and treatment outcomes of ovarian metastasis from gastric cancer.
Methods
This study included 155 female patients with unresectable advanced or recurrent gastric cancer at the Kochi Medical School between January 2007 and December 2021. A review of patients with ovarian metastasis was conducted, and their clinicopathological information and survival outcomes were compared with respect to ovarian metastasis.
Results
Fifteen patients were diagnosed with ovarian metastasis from gastric cancer with a median age of 54 years (range: 30–87 years) and an incidence of 9.7%. The median age of patients who developed ovarian metastasis was significantly lower those without ovarian metastasis (54 years vs. 71 years, P = 0.014). The median survival time (MST) for 15 patients with unresectable advanced gastric cancer who developed ovarian metastasis was 21.4 months (range: 0.2–41.4 months). The MST for 15 patients who underwent surgical resection and systemic drug treatment including chemotherapy to ovarian metastasis was significantly higher than those who received systemic drug treatment alone (28.1 months vs. 10.0 months; P = 0.021).
Conclusion
Ovarian metastasis was found in 9.7% of female patients with unresectable advanced or recurrent gastric cancer and in younger patients than in those without ovarian metastasis. Multidisciplinary treatment, including surgical resection and systemic drug treatment for ovarian metastasis from gastric cancer, may benefit selected patients.
Similar content being viewed by others
References
Nashimoto A, Akazawa K, Isobe Y, Miyashiro I, Katai H, Kodera Y, Tsujitani S, Seto Y, Furukawa H, Oda I, Ono H, Tanabe S, Kaminishi M (2013) Gastric cancer treated in 2002 in Japan: 2009 annual report of the JGCA nationwide registry. Gastric Cancer 16:1–27
Fidler MM, Gupta S, Soerjomataram I, Ferlay J, Steliarova-Foucher E, Bray F (2017) Cancer incidence and mortality among young adults aged 20–39 years worldwide in 2012: a population-based study. Lancet Oncol 18:1579–1589
Japanese Gastric Cancer Association (2011) Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer 14:101–112
Namikawa T, Ishida N, Tsuda S, Fujisawa K, Munekage E, Iwabu J, Munekage M, Uemura S, Tsujii S, Tamura T, Yatabe T, Maeda H, Kitagawa H, Kobayashi M, Hanazaki K (2019) Prognostic significance of serum alkaline phosphatase and lactate dehydrogenase levels in patients with unresectable advanced gastric cancer. Gastric Cancer 22:684–691
Aurello P, Berardi G, Antolino L, Antonelli G, Rampini A, Moschetta G, Ramacciato G (2018) Is a surgical approach justified in metachronous Krukenberg tumor from gastric cancer? A systematic review. Oncol Res Treat 41:644–649
Krukenberg FE (1896) Uber Das Fibrosarcoma ovarii mucocellulare (carcinomatodes). Arch Gynak 50:287–321
Qiu L, Yang T, Shan XH, Hu MB, Li Y (2011) Metastatic factors for Krukenberg tumor: a clinical study on 102 cases. Med Oncol 28:1514–1519
Cho JH, Lim JY, Choi AR, Choi SM, Kim JW, Choi SH, Cho JY (2015) Comparison of surgery plus chemotherapy and palliative chemotherapy alone for advanced gastric cancer with Krukenberg tumor. Cancer Res Treat 47:697–705
Japanese Gastric Cancer Association (2021) Japanese gastric cancer treatment guidelines 2018 5th edition. Gastric Cancer 24:1–21.
Bang YJ, Van Cutsem E, Feyereislova A, Chung HC, Shen L, Sawaki A, Lordick F, Ohtsu A, Omuro Y, Satoh T, Aprile G, Kulikov E, Hill J, Lehle M, Rüschoff J, Kang YK, Investigators TT (2010) Trastuzumab in combination with chemotherapy versus chemotherapy alone for treatment of HER2-positive advanced gastric or gastro-oesophageal junction cancer (ToGA): a phase 3, open-label, randomised controlled trial. Lancet 376:687–697
Koizumi W, Narahara H, Hara T, Takagane A, Akiya T, Takagi M, Miyashita K, Nishizaki T, Kobayashi O, Takiyama W, Toh Y, Nagaie T, Takagi S, Yamamura Y, Yanaoka K, Orita H, Takeuchi M (2008) S-1 plus cisplatin versus S-1 alone for first-line treatment of advanced gastric cancer (SPIRITS trial): a phase III trial. Lancet Oncol 9:215–221
Boku N, Yamamoto S, Fukuda H, Shirao K, Doi T, Sawaki A, Koizumi W, Saito H, Yamaguchi K, Takiuchi H, Nasu J, Ohtsu A, Gastrointestinal Oncology Study Group of the Japan Clinical Oncology Group (2009) Fluorouracil versus combination of irinotecan plus cisplatin versus S-1 in metastatic gastric cancer: a randomised phase 3 study. Lancet Oncol 10:1063–1069.
Wang J, Shi YK, Wu LY, Wang JW, Yang S, Yang JL, Zhang HZ, Liu SM (2008) Prognostic factors for ovarian metastases from primary gastric cancer. Int J Gynecol Cancer 18:825–832
Kubeček O, Laco J, Špaček J, Petera J, Kopecký J, Kubečková A, Filip S (2017) The pathogenesis, diagnosis, and management of metastatic tumors to the ovary: a comprehensive review. Clin Exp Metastasis 34:295–307
Kakushima N, Kamoshida T, Hirai S, Hotta S, Hirayama T, Yamada J, Ueda K, Sato M, Okumura M, Shimokama T, Oka Y (2003) Early gastric cancer with Krukenberg tumor and review of cases of intramucosal gastric cancers with Krukenberg tumor. J Gastroenterol 38:1176–1180
Fujimoto D, Hirono Y, Goi T, Yamaguchi A (2016) Sigmoid colonic metastasis by lymphatic spread occurring with unilateral Krukenberg tumor considered to be caused by stage IA early gastric cancer: a case report. Oncol Lett 11:668–672
Jeung YJ, Ok HJ, Kim WG, Kim SH, Lee TH (2015) Krukenberg tumors of gastric origin versus colorectal origin. Obstet Gynecol Sci 58:32–39
Seow-En I, Hwarng G, Tan GHC, Ho LML, Teo MCC (2018) Palliative surgery for Krukenberg tumors −12-year experience and review of the literature. World J Clin Oncol 9:13–19
Wu XJ, Yuan P, Li ZY, Bu ZD, Zhang LH, Wu AW, Zong XL, Li SX, Shan F, Ji X, Ren H, Ji JF (2013) Cytoreductive surgery and hyperthermic intraperitoneal chemotherapy improves the survival of gastric cancer patients with ovarian metastasis and peritoneal dissemination. Tumour Biol 34:463–469
Rosa F, Marrelli D, Morgagni P, Cipollari C, Vittimberga G, Framarini M, Cozzaglio L, Pedrazzani C, Berardi S, Baiocchi GL, Roviello F, Portolani N, de Manzoni G, Costamagna G, Doglietto GB, Pacelli F (2016) Krukenberg tumors of gastric origin: the rationale of surgical resection and perioperative treatments in a multicenter western experience. World J Surg 40:921–928
Yan D, Du Y, Dai G, Huang L, Xu Q, Yu P (2018) Management of synchronous Krukenberg tumors from gastric cancer: a single-center experience. J Cancer 9:4197–4203
F, Li Y, Li W, Kang W, Liu H, Ma S, Xie Y, Zhong Y, Xu Q, Wang B, Xue L, Tian Y, (2019) Metastasectomy improves the survival of gastric cancer patients with Krukenberg tumors: a retrospective analysis of 182 patients. Cancer Manag Res 11:10573–10580
Sandhu S, Arafat O, Patel H, Lall C (2012) Krukenberg tumor: a rare cause of ovarian torsion. J Clin Imaging Sci 2:6
Lu LC, Shao YY, Hsu CH, Hsu C, Cheng WF, Lin YL, Cheng AL, Yeh KH (2012) Metastasectomy of Krukenberg tumors may be associated with survival benefits in patients with metastatic gastric cancer. Anticancer Res 32:3397–3401
Cheong JH, Hyung WJ, Chen J, Kim J, Choi SH, Noh SH (2004) Surgical management and outcome of metachronous Krukenberg tumors from gastric cancer. J Surg Oncol 87:39–45
Peng W, Hua RX, Jiang R, Ren C, Jia YN, Li J, Guo WJ (2013) Surgical treatment for patients with Krukenberg tumor of stomach origin: clinical outcome and prognostic factors analysis. PLoS ONE 8:e68227
Camargo MC, Goto Y, Zabaleta J, Morgan DR, Correa P, Rabkin CS (2012) Sex hormones, hormonal interventions, and gastric cancer risk: a meta-analysis. Cancer Epidemiol Biomarkers Prev 21:20–38
Ur Rahman MS, Cao J (2016) Estrogen receptors in gastric cancer: advances and perspectives. World J Gastroenterol 22:2475–2482
Li SQ, Zhang KC, Li JY, Liang WQ, Gao YH, Qiao Z, Xi HQ, Chen L (2020) Establishment and validation of a nomogram to predict the risk of ovarian metastasis in gastric cancer: based on a large cohort. World J Clin Cases 8:4331–4341
Wang B, Tang Q, Xu L, Teng X, Ding W, Ren G, Wang X (2021) A comparative study of RTK gene status between primary tumors, lymph-node metastases, and Krukenberg tumors. Mod Pathol 34:42–50
Wang B, Sun K, Zou Y (2017) Comparison of a panel of biomarkers between gastric primary cancer and the paired Krukenberg tumor. Appl Immunohistochem Mol Morphol 25:639–644
Van Cutsem E, Bang YJ, Feng-Yi F, Xu JM, Lee KW, Jiao SC, Chong JL, López-Sanchez RI, Price T, Gladkov O, Stoss O, Hill J, Ng V, Lehle M, Thomas M, Kiermaier A, Rüschoff J (2015) HER2 screening data from ToGA: targeting HER2 in gastric and gastroesophageal junction cancer. Gastric Cancer 18:476–484
Boku N (2014) HER2-positive gastric cancer. Gastric Cancer 17:1–12
Wilke H, Muro K, Van Cutsem E, Oh SC, Bodoky G, Shimada Y, Hironaka S, Sugimoto N, Lipatov O, Kim TY, Cunningham D, Rougier P, Komatsu Y, Ajani J, Emig M, Carlesi R, Ferry D, Chandrawansa K, Schwartz JD, Ohtsu A and RAINBOW Study Group (2014) Ramucirumab plus paclitaxel versus placebo plus paclitaxel in patients with previously treated advanced gastric or gastro-oesophageal junction adenocarcinoma (RAINBOW): a double-blind, randomised phase 3 trial. Lancet Oncol 15:1224–1235
Kang YK, Boku N, Satoh T, Ryu MH, Chao Y, Kato K, Chung HC, Chen JS, Muro K, Kang WK, Yeh KH, Yoshikawa T, Oh SC, Bai LY, Tamura T, Lee KW, Hamamoto Y, Kim JG, Chin K, Oh DY, Minashi K, Cho JY, Tsuda M, Chen LT (2017) Nivolumab in patients with advanced gastric or gastro-oesophageal junction cancer refractory to, or intolerant of, at least two previous chemotherapy regimens (ONO-4538-12, ATTRACTION-2): a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet 390:2461–2471
Namikawa T, Marui A, Yokota K, Fujieda Y, Munekage M, Uemura S, Maeda H, Kitagawa H, Kobayashi M, Hanazaki K (2021) Successful conversion surgery for advanced gastric cancer with multiple liver metastases following ramucirumab plus paclitaxel combination treatment. In Vivo 35:2929–2935
Acknowledgements
We would like to acknowledge the contributions of our colleagues from the Department of Surgery, Kochi Medical School.
Author information
Authors and Affiliations
Contributions
Study conception and design: Tsutomu Namikawa.
Acquisition of data: Tsutomu Namikawa, Akira Marui, Keiichiro Yokota, Yasuhiro Kawanishi, Masaya Munekage, Sunao Uemura, Hiroyuki Kitagawa, Michiya Kobayashi.
Analysis and interpretation of data: Tsutomu Namikawa and Hiromichi Maeda.
Drafting of manuscript: Tsutomu Namikawa.
Critical revision of manuscript: Tsutomu Namikawa and Kazuhiro Hanazaki.
Corresponding author
Ethics declarations
Ethics approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Namikawa, T., Marui, A., Yokota, K. et al. Frequency and therapeutic strategy for patients with ovarian metastasis from gastric cancer. Langenbecks Arch Surg 407, 2301–2308 (2022). https://doi.org/10.1007/s00423-022-02543-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00423-022-02543-3