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Correlation Between Tumor Vasculogenic Mimicry and Poor Prognosis of Human Digestive Cancer Patients: A Systematic Review and Meta-Analysis

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Pathology & Oncology Research

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Abstract

Vasculogenic mimicry (VM) is a new pattern of blood supplement independent of endothelial vessels, which is related with tumor invasion, metastasis and prognosis. However, the role of VM in the prognosis of cancer patients is controversial. This study aimed to perform a meta-analysis of the published data to attempt to clarify the prognostic value of VM in the digestive cancer. Relevant studies were retrieved from the PubMed, Web of Science, Cochrane Library, Chinese National Knowledge Infrastructure and VIP databases published before March 29, 2018. Studies were included if they detected VM in the digestive cancer and analyzed the overall survival (OS) or disease-free survival (DFS) according to VM status. Two independent reviewers screened the studies, extracted data, and evaluated the quality of included studies with the Newcastle-Ottawa scale. Meta-analysis was performed using STATA 12.0 software. A total of 22 studies with 2411 patients were included in this meta-analysis. Meta-analysis showed that VM was related with the poor OS (HR = 2.30, 95% CI: 2.06–2.56, P < 0.001) and DFS (HR = 2.60, 95% CI: 2.07–3.27, P < 0.001) of patients with digestive cancer. Subgroup analysis showed VM was related with tumor differentiation, lymph node metastasis and TNM stage. Moreover, the present meta-analysis was reliable, and there was no obvious publication bias. This meta-analysis suggested that VM was a poor prognosis of digestive cancer patients. Further large and well-designed studies are required.

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References

  1. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A (2015) Global cancer statistics, 2012. CA Cancer J Clin 65(2):87–108

    Article  PubMed  Google Scholar 

  2. Jemal A, Siegel R, Xu J, Ward E (2010) Cancer statistics, 2010. CA Cancer J Clin 60(5):277–300

    Article  PubMed  Google Scholar 

  3. Qiao L, Liang N, Zhang J, Xie J, Liu F, Xu D, Yu X, Tian Y (2015) Advanced research on vasculogenic mimicry in cancer. J Cell Mol Med 19(2):315–326

    Article  PubMed  PubMed Central  Google Scholar 

  4. Maniotis AJ, Folberg R, Hess A, Seftor EA, Gardner LM, Pe'er J, Trent JM, Meltzer PS, Hendrix MJ (1999) Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am J Pathol 155(3):739–752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Williamson SC, Metcalf RL, Trapani F, Mohan S, Antonello J, Abbott B, Leong HS, Chester CP, Simms N, Polanski R, Nonaka D, Priest L, Fusi A, Carlsson F, Carlsson A, Hendrix MJ, Seftor RE, Seftor EA, Rothwell DG, Hughes A, Hicks J, Miller C, Kuhn P, Brady G, Simpson KL, Blackhall FH, Dive C (2016) Vasculogenic mimicry in small cell lung cancer. Nat Commun 7:13322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Guo Q, Yuan Y, Jin Z, Xu T, Gao Y, Wei H, Li C, Hou W, Hua B (2016) Association between Tumor Vasculogenic Mimicry and the Poor Prognosis of Gastric Cancer in China: An Updated Systematic Review and Meta-Analysis. Biomed Res Int 2016:2408645

    PubMed  PubMed Central  Google Scholar 

  7. Baeten CI, Hillen F, Pauwels P, de Bruine AP, Baeten CG (2009) Prognostic role of vasculogenic mimicry in colorectal cancer. Dis Colon Rectum 52(12):2028–2035

    Article  PubMed  Google Scholar 

  8. Shen Y, Quan J, Wang M, Li S, Yang J, Lv M, Chen Z, Zhang L, Zhao X, Yang J (2017) Tumor vasculogenic mimicry formation as an unfavorable prognostic indicator in patients with breast cancer. Oncotarget 8(34):56408–56416

    PubMed  PubMed Central  Google Scholar 

  9. Shirakawa K, Wakasugi H, Heike Y, Watanabe I, Yamada S, Saito K, Konishi F (2002) Vasculogenic mimicry and pseudo-comedo formation in breast cancer. Int J Cancer 99(6):821–828

    Article  CAS  PubMed  Google Scholar 

  10. Yang JP, Liao YD, Mai DM, Xie P, Qiang YY, Zheng LS, Wang MY, Mei Y, Meng DF, Xu L, Cao L, Yang Q, Yang XX, Wang WB, Peng LX, Huang BJ, Qian CN (2016) Tumor vasculogenic mimicry predicts poor prognosis in cancer patients: a meta-analysis. Angiogenesis 19(2):191–200

    Article  CAS  PubMed  Google Scholar 

  11. Sun B, Zhang S, Zhao X, Zhang W, Hao X (2004) Vasculogenic mimicry is associated with poor survival in patients with mesothelial sarcomas and alveolar rhabdomyosarcomas. Int J Oncol 25(6):1609–1614

    PubMed  Google Scholar 

  12. van Beurden A, Schmitz RF, van Dijk CM, Baeten CI (2012) Periodic acid Schiff loops and blood lakes associated with metastasis in cutaneous melanoma. Melanoma Res 22(6):424–429

    Article  PubMed  Google Scholar 

  13. Knobloch K, Yoon U, Vogt PM (2011) Preferred reporting items for systematic reviews and meta-analyses (PRISMA) statement and publication bias. J Craniomaxillofac Surg 39(2):91–92

    Article  PubMed  Google Scholar 

  14. Moher D, Liberati A, Tetzlaff J, Altman DG (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol 62(10):1006–1012

    Article  PubMed  Google Scholar 

  15. Jadad AR, Moore RA, Carroll D, Jenkinson C, Reynolds DJ, Gavaghan DJ, McQuay HJ (1996) Assessing the quality of reports of randomized clinical trials: is blinding necessary? Control Clin Trials 17(1):1–12

    Article  CAS  Google Scholar 

  16. Chai DM, Bao ZQ, Hu JG, Ma L, Feng ZZ, Tao YS (2013) Vasculogenic mimicry and aberrant expression of HIF-lalpha/E-cad are associated with worse prognosis of esophageal squamous cell carcinoma. J Huazhong Univ Sci Technolog Med Sci 33(3):385–391

    Article  CAS  PubMed  Google Scholar 

  17. Guzman G, Cotler SJ, Lin AY, Maniotis AJ, Folberg R (2007) A pilot study of vasculogenic mimicry immunohistochemical expression in hepatocellular carcinoma. Arch Pathol Lab Med 131(12):1776–1781

    PubMed  PubMed Central  Google Scholar 

  18. Li M, Gu Y, Zhang Z, Zhang S, Zhang D, Saleem AF, Zhao X, Sun B (2010) Vasculogenic mimicry: a new prognostic sign of gastric adenocarcinoma. Pathol Oncol Res 16(2):259–266

    Article  PubMed  Google Scholar 

  19. Li J, Ma XJ, Du XB, Feng G, Tan BX (2014) The influence of vasculogenic mimicry expression onprognosis of patients with primary liver cancer. Pract J Clin Med 11(02):102–106

  20. Li J (2016) The role of Cyclooxygenase-2 in gastic cancer vasculogenic mimicry and its molecular mechanism. Chinese master’s dissertation of Tianjin medical university

  21. Liao SP, Gao Q (2013) Expressions and clinical significance of vasculogenic mimicry and relatedprotein Mig-7 and MMP-2 in gastric carcinoma. J Cell Molecular Immunol 29(02):194–196

  22. Liu WB, Xu GL, Jia WD, Li JS, Ma JL, Chen K, Wang ZH, Ge YS, Ren WH, Yu JH, Wang W, Wang XJ (2011) Prognostic significance and mechanisms of patterned matrix vasculogenic mimicry in hepatocellular carcinoma. Med Oncol 28(Suppl 1):S228–S238

    Article  PubMed  Google Scholar 

  23. Lv J, Sun B, Sun H, Zhang Y, Sun J, Zhao X, Gu Q, Dong X, Che N (2017) Significance of Vasculogenic Mimicry Formation in Gastric Carcinoma. Oncol Res Treat 40(1–2):35–41

    Article  CAS  PubMed  Google Scholar 

  24. Shao B (2016) Correlation between the overexpression of LOXL2 and the metastasis and prognosic value in hepatocellar carcinoma. J Clin Exp Pathol 32(2):123–126

  25. Song WQ, Yu L, Wu SW, Tao YS (2013) Expression of vascular endothelial growth factor and its correlation with prognosis in esophageal squamous cell carcinoma. Chin J Gerontol 23:5855–5857

    Google Scholar 

  26. Song YY, Sun LD, Liu ML, Liu ZL, Chen F, Zhang YZ, Zheng Y, Zhang JP (2014) STAT3, p-STAT3 and HIF-1alpha are associated with vasculogenic mimicry and impact on survival in gastric adenocarcinoma. Oncol Lett 8(1):431–437

    Article  PubMed  PubMed Central  Google Scholar 

  27. Sun B, Zhang S, Zhang D, Du J, Guo H, Zhao X, Zhang W, Hao X (2006) Vasculogenic mimicry is associated with high tumor grade, invasion and metastasis, and short survival in patients with hepatocellular carcinoma. Oncol Rep 16(4):693–698

    CAS  PubMed  Google Scholar 

  28. Sun W, Shen ZY, Zhang H, Fan YZ, Zhang WZ, Zhang JT, Lu XS, Ye C (2012) Overexpression of HIF-1 alpha in primary gallbladder carcinoma and its relation to vasculogenic mimicry and unfavourable prognosis. Oncol Rep 27(6):1990–2002

    CAS  PubMed  Google Scholar 

  29. Wang L, Lin L, Chen X, Sun L, Liao YL, Huang N, Liao WJ (2015) Metastasis-associated in colon cancer-1 promotes vasculogenic mimicry in gastric cancer by upregulating TWIST1/2. Oncotarget 6(13):11492–11506

    PubMed  PubMed Central  Google Scholar 

  30. Yang Z (2011) Preliminary study on the mimicry of angiogenesis in gastric cancer.. Chinese master’s dissertation of university of south China

  31. Yang ZH, Sun BC, Li YL, Zhao XL, Zhao XM, Gu Q, An JD, Dong XY, Liu F, Wang Y (2015) ZEB2 promotes vasculogenic mimicry by TGF-beta 1 induced epithelial-to-mesenchymal transition in hepatocellular carcinoma. Exp Mol Pathol 98(3):352–359

    Article  CAS  PubMed  Google Scholar 

  32. Yang J, Zhu DM, Zhou XG, Yin N, Zhang Y, Zhang ZX, Li DC, Zhou J (2017) HIF-2 alpha promotes the formation of vasculogenic mimicry in pancreatic cancer by regulating the binding of Twist1 to the VE-cadherin promoter. Oncotarget 8(29):47801–47815

    PubMed  PubMed Central  Google Scholar 

  33. Zhang JX, Zhang GX, Hu PP, Deng GD, Liu QQ, Qiao LL, Luo H, Zhang JD (2017) Vasculogenic mimicry is associated with increased tumor-infiltrating neutrophil and poor outcome in esophageal squamous cell carcinoma. Onco Targets Ther 10:2923–2930

    Article  PubMed  PubMed Central  Google Scholar 

  34. Zheng QH, Yang YH, Lin XF (2012) A preliminary study of vasculogenic mimicry in human gallbladder carcinoma and its clinical significance. J Fujian Med Univ 46(4):248–250

  35. Zhou L, Yu L, Feng ZZ, Gong XM, Cheng ZN, Yao N, Wang DN, Wu SW (2015) Aberrant Expression of Markers of Cancer Stem Cells in Gastric Adenocarcinoma and their Relationship to Vasculogenic Mimicry. Asian Pac J Cancer Prev 16(10):4177–4183

    Article  PubMed  Google Scholar 

  36. Zhu B, Zhou L, Yu L, Wu S, Song W, Gong X, Wang D (2017) Evaluation of the correlation of vasculogenic mimicry, ALDH1, KAI1 and microvessel density in the prediction of metastasis and prognosis in colorectal carcinoma. BMC Surg 17(1):47

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Cassidy RJ, Liu Y, Patel K, Zhong J, Steuer CE, Kooby DA, Russell MC, Gillespie TW, Landry JC (2017) Can we eliminate neoadjuvant chemoradiotherapy in favor of neoadjuvant multiagent chemotherapy for select stage II/III rectal adenocarcinomas: Analysis of the National Cancer Data base. Cancer 123(5):783–793

    Article  CAS  PubMed  Google Scholar 

  38. Delgado-Bellido D, Serrano-Saenz S, Fernandez-Cortes M, Oliver FJ (2017) Vasculogenic mimicry signaling revisited: focus on non-vascular VE-cadherin. Mol Cancer 16(1):65

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Li S, Meng W, Guan Z, Guo Y, Han X (2016) The hypoxia-related signaling pathways of vasculogenic mimicry in tumor treatment. Biomed Pharmacother 80:127–135

    Article  CAS  PubMed  Google Scholar 

  40. Sun W, Shen ZY, Zhang H, Fan YZ, Zhang WZ, Zhang JT, Lu XS, Ye C (2012) Overexpression of HIF-1alpha in primary gallbladder carcinoma and its relation to vasculogenic mimicry and unfavourable prognosis. Oncol Rep 27(6):1990–2002

    CAS  PubMed  Google Scholar 

  41. Du J, Sun B, Zhao X, Gu Q, Dong X, Mo J, Sun T, Wang J, Sun R, Liu Y (2014) Hypoxia promotes vasculogenic mimicry formation by inducing epithelial-mesenchymal transition in ovarian carcinoma. Gynecol Oncol 133(3):575–583

    Article  CAS  PubMed  Google Scholar 

  42. Hendrix MJ, Seftor EA, Meltzer PS, Gardner LM, Hess AR, Kirschmann DA, Schatteman GC, Seftor RE (2001) Expression and functional significance of VE-cadherin in aggressive human melanoma cells: role in vasculogenic mimicry. Proc Natl Acad Sci U S A 98(14):8018–8023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Wang H, Lin H, Pan J, Mo C, Zhang F, Huang B, Wang Z, Chen X, Zhuang J, Wang D, Qiu S (2016) Vasculogenic Mimicry in Prostate Cancer: The Roles of EphA2 and PI3K. J Cancer 7(9):1114–1124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Hao X, Sun B, Zhang S, Zhao X (2002) Microarray study of vasculogenic mimicry in bi-directional differentiation malignant tumor. Zhonghua Yi Xue Za Zhi 82(19):1298–1302

    PubMed  Google Scholar 

  45. Stacker SA, Achen MG (2013) The VEGF signaling pathway in cancer: the road ahead. Chin J Cancer 32(6):297–302

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Sun B, Zhang D, Zhao N, Zhao X (2017) Epithelial-to-endothelial transition and cancer stem cells: two cornerstones of vasculogenic mimicry in malignant tumors. Oncotarget 8(18):30502–30510

    Article  PubMed  Google Scholar 

  47. Liu T, Sun B, Zhao X, Li Y, Zhao X, Liu Y, Yao Z, Gu Q, Dong X, Shao B, Lin X, Liu F, An J (2015) USP44+ Cancer Stem Cell Subclones Contribute to Breast Cancer Aggressiveness by Promoting Vasculogenic Mimicry. Mol Cancer Ther 14(9):2121–2131

    Article  CAS  PubMed  Google Scholar 

  48. Wu S, Yu L, Wang D, Zhou L, Cheng Z, Chai D, Ma L, Tao Y (2012) Aberrant expression of CD133 in non-small cell lung cancer and its relationship to vasculogenic mimicry. BMC Cancer 12:535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Liu Y, Sun B, Liu T, Zhao X, Wang X, Li Y, Meng J, Gu Q, Liu F, Dong X, Liu P, Sun R, Zhao N (2016) Function of AURKA protein kinase in the formation of vasculogenic mimicry in triple-negative breast cancer stem cells. OncoTargets and therapy 9:3473–3484

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Wu HB, Yang S, Weng HY, Chen Q, Zhao XL, Fu WJ, Niu Q, Ping YF, Wang JM, Zhang X, Yao XH, Bian XW (2017) Autophagy-induced KDR/VEGFR-2 activation promotes the formation of vasculogenic mimicry by glioma stem cells. Autophagy 13(9):1528–1542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (Grant No. 81572394), the Natural Science Foundation of Zhangzhou, Fujian, China (grant No. ZZ2017J36) and the Youth Nursery Foundation of the Affiliated Southeast Hospital of Xiamen University, Zhangzhou, Fujian, China (grant No. 16Y019).

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Correspondence to Dong-Yan Shen or Jia-Rong Meng.

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Supplemental Figure 1

Forest plot showing the combined relative HR for overall survival based on region (A), tumor types (B), VM assay methods (C), the number of case (D), the follow-up time (E) and the quality (F). (PNG 2069 kb)

High resolution image (TIF 2871 kb)

Supplemental Figure 2

Forest plot showing the relationship between VM and the clinicopathological features of patients with digestive cancer including gender (A), age (B), tumor size (C), differentiation (D), lymph node metastasis (E) and TNM stage (F). (PNG 796 kb)

High resolution image (TIF 1081 kb)

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Ren, HY., Shen, JX., Mao, XM. et al. Correlation Between Tumor Vasculogenic Mimicry and Poor Prognosis of Human Digestive Cancer Patients: A Systematic Review and Meta-Analysis. Pathol. Oncol. Res. 25, 849–858 (2019). https://doi.org/10.1007/s12253-018-0496-3

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  • DOI: https://doi.org/10.1007/s12253-018-0496-3

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