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Survival Outcomes in Stage IV Gastric Cancer Patients with Krukenberg Tumors: A Systematic Review and Meta Analysis

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Abstract

Background

Stage IV gastric cancer patients with Krukenberg tumors typically exhibit poor survival outcomes, often less than 2 years. The management of this tumor subgroup remains non-standardized, and the impact of oophorectomy on survival remains uncertain. In this study, we systematically analyzed survival outcomes among gastric cancer patients with ovarian metastases who underwent standard chemotherapy, surgical resection of ovarian metastases, or combined chemotherapy and surgery.

Methods

We conducted a systematic review and meta-analysis of randomized controlled trials and observational studies retrieved from MEDLINE (PubMed), Embase, and the Cochrane Library until January 25, 2024, applying the Boolean logic. Participants included individuals with pathologically and radiologically confirmed ovarian metastasis or clinically symptomatic cases with imaging evidence. Statistical analyses were performed using R (v.4.3.2., Vienna). The study was registered with PROSPERO (ID-CRD42023488373).

Results

A total of 1502 patients from 17 retrospective studies were pooled for analysis of overall survival (OS) outcomes. The OS in the standard chemotherapy cohort, as determined by the random effects model, was 6.708 months (95% CI 3.867 to 9.548; P<0.0001), with non-significant heterogeneity (I2 = 5.5%). In the surgical resection cohort, OS was 12.786 months (95% CI 6.9 to 18.671; P<0.0001), with low heterogeneity (I2 = 0%). In the combined chemotherapy and surgical resection cohort, OS was 16.228 months (95% CI 12.254 to 20.202), with insignificant heterogeneity (I2 = 0%).

Conclusion

This meta-analysis offers key insights into survival outcomes associated with different therapeutic modalities in gastric cancer with Krukenberg metastases. It provides valuable evidence for clinical decision-making and future research directions. While the combined approach of chemotherapy and surgery demonstrates the highest effect size for OS, careful consideration of patient-centric approaches is essential in the oncological care landscape.

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Data Availability

No datasets were generated or analyzed during the current study.

References

  1. Uyeturk U, Arslan SH, Bal O, Arslan UY, Oksuzoglu OBC. Isolated ovarian metastasis of gastric cancer: Krukenberg tumor. Contemp Oncol Onkol. 2013;17(6):515–9.

    Google Scholar 

  2. Finkelstein SD, Sayegh R, Christensen S, Swalsky PA. Genotypic classification of colorectal adenocarcinoma. Biologic behavior correlates with K‐ras‐2 mutation type. Cancer. 1993;71(12):3827–38.

    Article  CAS  PubMed  Google Scholar 

  3. Kim JH, Cha HJ, Kim K-R, Kim K. Primary ovarian signet ring cell carcinoma: a rare case report. Mol Clin Oncol. 2018;9(2):211–4.

    PubMed  PubMed Central  Google Scholar 

  4. Kim SH, Kim WH, Park KJ, Lee JK, Kim JS. CT and MR findings of Krukenberg tumors: comparison with primary ovarian tumors. J Comput Assist Tomogr. 1996;20(3):393–8.

    Article  CAS  PubMed  Google Scholar 

  5. Lionetti R, De Luca M, Travaglino A, Raffone A, Insabato L, Saccone G, et al. Treatments and overall survival in patients with Krukenberg tumor. Arch Gynecol Obstet. 2019;300:15–23.

    Article  PubMed  Google Scholar 

  6. Lyngdoh BS, Dey B, Mishra J, Marbaniang E. Krukenberg tumor Autops Case Reports. 2020;10: e2020163.

    Article  Google Scholar 

  7. Kovalev V, Tariq A. c World J Color Surg. 2023;12(2):31–5.

    Article  Google Scholar 

  8. Gligorievski A. Appearance of Krukenberg tumor from gastric carcinoma, ultrasound and computed tomography evaluation. Dig Med Res. 2018;1:3.

    Article  Google Scholar 

  9. Chen C, Ge X, Zhao Y, Wang D, Ling L, Zheng S, et al. Molecular alterations in metastatic ovarian cancer from gastrointestinal cancer. Front Oncol. 2020;10: 605349.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Dundr P, Singh N, Nožičková B, Němejcová K, Bártů M, Stružinská I. Primary mucinous ovarian tumors vs. ovarian metastases from gastrointestinal tract pancreas and biliary tree: a review of current problematics. Diagn Pathol. 2021;16(1):1–17.

    Article  Google Scholar 

  11. Hirono M, Taniyama K, Matsuki K, Nakagami K, Niimoto M, Hattori T. Clinico-pathological studies on ovarian metastasis from gastric cancer. Jpn J Surg. 1983;13:25–31.

    Article  CAS  PubMed  Google Scholar 

  12. Jun S-Y, Park JK. Metachronous ovarian metastases following resection of the primary gastric cancer. J Gastric Cancer. 2011;11(1):31–7.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;29:372.

    Google Scholar 

  14. PROSPERO. [Protocol] Survival outcomes in ovarian metastasis from gastric cancer: an updated meta-analysis [Internet]. 2023. Available from: https://www.crd.york.ac.uk/prospero/display_record.php?RecordID=488373

  15. Kobayashi O, Sugiyama Y, Cho H, Tsuburaya A, Sairenji M, Motohashi H, et al. Clinical and pathological study of gastric cancer with ovarian metastasis. Int J Clin Oncol. 2003;8:67–71.

    Article  PubMed  Google Scholar 

  16. Lee M, Paek J, Lee SH, Yim GW, Kim SW, Kim S, et al. Feasibility and surgical outcomes of laparoscopic metastasectomy in the treatment of ovarian metastases from gastric cancer. Int J Gynecol Cancer. 2011;21(7):1306–11.

    PubMed  Google Scholar 

  17. Wang J, Shi Y, Wu L, Wang J, Yang S, Yang J, et al. Prognostic factors for ovarian metastases from primary gastric cancer. Int J Gynecol Cancer. 2008;18(4):825–32.

    Article  CAS  PubMed  Google Scholar 

  18. Cho JH, Lim JY, Choi AR, Choi SM, Kim JW, Choi SH, et al. Comparison of surgery plus chemotherapy and palliative chemotherapy alone for advanced gastric cancer with Krukenberg tumor. Cancer Res Treat Off J Korean Cancer Assoc. 2018;50(1):302.

    Google Scholar 

  19. Kim HK, Heo DS, Bang Y-J, Kim NK. Prognostic factors of Krukenberg’s tumor. Gynecol Oncol. 2001;82(1):105–9.

    Article  CAS  PubMed  Google Scholar 

  20. Cheong JH, Hyung WJ, Chen J, Kim J, Choi SH, Noh SH. Surgical management and outcome of metachronous Krukenberg tumors from gastric cancer. J Surg Oncol. 2004;87(1):39–45.

    Article  PubMed  Google Scholar 

  21. Cheong JH, Hyung WJ, Chen J, Kim J, Choi SH, Noh SH. Survival benefit of metastasectomy for Krukenberg tumors from gastric cancer. Gynecol Oncol. 2004;94(2):477–82.

    Article  PubMed  Google Scholar 

  22. Lu L-C, Shao Y-Y, Hsu C-H, Hsu C, Cheng W-F, Lin Y-L, et al. Metastasectomy of Krukenberg tumors may be associated with survival benefits in patients with metastatic gastric cancer. Anticancer Res. 2012;32(8):3397–401.

    PubMed  Google Scholar 

  23. Feng Q, Pei W, Zheng Z-X, Bi J-J, Yuan X-H. Clinicopathologic characteristics and prognostic factors of 63 gastric cancer patients with metachronous ovarian metastasis. Cancer Biol Med. 2013;10(2):86.

    PubMed  PubMed Central  Google Scholar 

  24. Peng W, Hua R-X, Jiang R, Ren C, Jia Y-N, Li J, et al. Surgical treatment for patients with Krukenberg tumor of stomach origin: clinical outcome and prognostic factors analysis. PLoS ONE. 2013;8(7): e68227.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Brieau B, Auzolle C, Pozet A, Tougeron D, Bouché O, Soibinet P, et al. Efficacy of modern chemotherapy and prognostic factors in patients with ovarian metastases from gastric cancer: a retrospective AGEO multicentre study. Dig Liver Dis. 2016;48(4):441–5.

    Article  CAS  PubMed  Google Scholar 

  26. Rosa F, Marrelli D, Morgagni P, Cipollari C, Vittimberga G, Framarini M, et al. Krukenberg tumors of gastric origin: the rationale of surgical resection and perioperative treatments in a multicenter western experience. World J Surg. 2016;40:921–8.

    Article  PubMed  Google Scholar 

  27. Yu P, Huang L, Cheng G, Yang L, Dai G, Ying J, et al. Treatment strategy and prognostic factors for Krukenberg tumors of gastric origin: report of a 10-year single-center experience from China. Oncotarget. 2017;8(47):82558.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Yan D, Du Y, Dai G, Huang L, Xu Q, Yu P. Management of synchronous krukenberg tumors from gastric cancer: a single-center experience. J Cancer. 2018;9(22):4197.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Ma F, Li Y, Li W, Kang W, Liu H, Ma S, et al. Metastasectomy improves the survival of gastric cancer patients with Krukenberg tumors: a retrospective analysis of 182 patients. Cancer Manag Res. 2019;10573–80.

  30. Fang J, Huang X, Chen X, Xu Q, Chai T, Huang L, et al. Efficacy of chemotherapy combined with surgical resection for gastric cancer with synchronous ovarian metastasis: a propensity score matching analysis. Cancer Med. 2023;12(16):17126–38.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Zhang C, Hou W, Huang J, Yin S, Wang P, Zhang Z, et al. Effects of metastasectomy and other factors on survival of patients with ovarian metastases from gastric cancer: a systematic review and meta-analysis. J Cell Biochem. 2019;120(9):14486–98.

    Article  CAS  PubMed  Google Scholar 

  32. Xie H, Erickson BJ, Sheedy SP, Yin J, Hubbard JM. The diagnosis and outcome of Krukenberg tumors. J Gastrointest Oncol. 2021;12(2):226.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Yang L-P, Wang Z-X, He M-M, Wu H-X, Yuan S-Q, Wang W, et al. A real-world evidence of efficacy of palliative gastrectomy plus chemotherapy in metastatic gastric cancer patients. Cancer Manag Res. 2019;3993–4003.

  34. Yang SW, Kim MG, Lee JH, Kwon SJ. Role of metastasectomy on overall survival of patients with metastatic gastric cancer. J Gastric Cancer. 2013;13(4):226–31.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Peng P, Liu X, Yang L, Gu Z, Cai L, Liu H. Systematically prognostic analyses of gastric cancer patients with ovarian metastasis. Genet Res (Camb). 2023;2023: e7.

    Article  Google Scholar 

  36. Namikawa T, Marui A, Yokota K, Kawanishi Y, Munekage M, Uemura S, et al. Frequency and therapeutic strategy for patients with ovarian metastasis from gastric cancer. Langenbeck’s Arch Surg. 2022;407(6):2301–8.

    Article  Google Scholar 

  37. Aurello P, Berardi G, Antolino L, et al. Is a surgical approach justified in metachronous Krukenberg tumor from gastric cancer? A systematic review Oncol Res Treat. 2018;41(10):644–9. https://doi.org/10.1159/000490956.

    Article  PubMed  Google Scholar 

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Contributions

All authors contributed to this manuscript equally. A.S. is the supervisor/guarantor.

Corresponding author

Correspondence to Anwaar Saeed.

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Conflict of Interest

Anwaar Saeed reports a leadership role with Autem therapeutics, Exelixis, KAHR Medical, and Bristol-Myers Squibb; consulting or advisory board role with AstraZeneca, Bristol-Myers Squibb, Merck, Exelixis, Pfizer, Xilio Therapeutics, Taiho, Amgen, Autem Therapeutics, KAHR Medical, and Daiichi Sankyo; institutional research funding from AstraZeneca, Bristol-Myers Squibb, Merck, Clovis, Exelixis, Actuate Therapeutics, Incyte Corporation, Daiichi Sankyo, Five Prime Therapeutics, Amgen, Innovent Biologics, Dragonfly Therapeutics, Oxford Biotherapeutics, Arcus Therapeutics, and KAHR Medical; and participation as a data safety monitoring board chair for Arcus Therapeutics. The remaining authors have no relevant financial interests to disclose.

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Anwar, J., Abdelhakeem, A., Khan, M.S. et al. Survival Outcomes in Stage IV Gastric Cancer Patients with Krukenberg Tumors: A Systematic Review and Meta Analysis. J Gastrointest Canc (2024). https://doi.org/10.1007/s12029-024-01068-w

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