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Polymorphisms of vascular endothelial growth factor and recurrent implantation failure: a systematic review and meta-analysis

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Abstract

Purpose

To investigate the associations between polymorphisms of vascular endothelial growth factor (VEGF) with recurrent implantation failure (RIF).

Methods

We performed the systematic review and meta-analysis by searching databases of PubMed, EMBASE, OVID, and CNKI (China National Knowledge Infrastructure) for studies that evaluated the associations between VEGF polymorphisms with RIF. Meta-analysis was performed if the polymorphism was studied by more than two case–control studies. Data were analyzed using R software. Odds ratios (ORs) with 95% confidence intervals (CIs) were reported to assess the associations.

Results

Nine VEGF polymorphisms (−1154G > A, −460T > C, +405G > C, −7C > T, −634C > G, −2578C > A, +936C > T, 5C > T, −583C > T) were systematically reviewed. Meta-analysis was performed on VEGF −1154 G > A polymorphism. Three case–control studies consisted of 683 women were included in the quantitative meta-analysis (305 RIF patients and 378 controls). Results showed that VEGF −1154A allele was significantly associated with RIF (OR 1.39, 95% CI 1.08–1.78, P-value = 0.01). The dominant genetic model showed that VEGF 1154AA plus VEGF 1154AG genotypes were more frequent in RIF patients than VEGF 1154GG genotype (OR 1.56, 95% CI 1.10–2.20, P-value = 0.01). However, the result under the recessive genetic model showed no significant difference (OR 1.67, 95% CI 0.92–3.03, P-value = 0.09).

Conclusion

VEGF −1154A allele may serve as one of the predisposing factors of RIF. Women with VEGF 1154 AA/GA genotypes were at higher risk of RIF. However, we should consider the haplotype effect of VEGF polymorphisms in future studies.

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Data availability

The data sets used and analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Vagnini LD, Renzi A, Petersen B et al (2019) Association between estrogen receptor 1 (ESR1) and leukemia inhibitory factor (LIF) polymorphisms can help in the prediction of recurrent implantation failure. Fertil Steril 111(3):527–534

    Article  CAS  PubMed  Google Scholar 

  2. Coughlan C, Ledger W, Wang Q et al (2014) Recurrent implantation failure: definition and management. Reprod Biomed Online 28(1):14–38

    Article  CAS  PubMed  Google Scholar 

  3. Zeng H, He D, Zhao Y, Liu NG, Xie H. Association between MTHFR polymorphisms (MTHFR C677T, MTHFR A1298C) and recurrent implantation failure: a systematic review and meta-analysis. Arch Gynecol Obstet, 2020.

  4. Polanski LT, Baumgarten MN, Quenby S et al (2014) What exactly do we mean by “recurrent implantation failure”? A systematic review and opinion. Reprod Biomed Online 28(4):409–423

    Article  PubMed  Google Scholar 

  5. Fang Y, Yu S, Ma Y et al (2013) Association of Dll4/notch and HIF-1a -VEGF signaling in the angiogenesis of missed abortion. PLoS ONE 8(8):e70667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Meher A, Sundrani D, Joshi S (2015) Maternal nutrition influences angiogenesis in the placenta through peroxisome proliferator activated receptors: a novel hypothesis. Mol Reprod Dev 82(10):726–734

    Article  CAS  PubMed  Google Scholar 

  7. Ferrara N (2004) Vascular endothelial growth factor as a target for anticancer therapy. Oncologist 9(Suppl 1):2–10

    Article  CAS  PubMed  Google Scholar 

  8. De Falco S (2012) The discovery of placenta growth factor and its biological activity. Exp Mol Med 44(1):1–9

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Hiratsuka S, Kataoka Y, Nakao K et al (2005) Vascular endothelial growth factor A (VEGF-A) is involved in guidance of VEGF receptor-positive cells to the anterior portion of early embryos. Mol Cell Biol 25(1):355–363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Ferrara N (2004) Vascular endothelial growth factor: basic science and clinical progress. Endocr Rev 25(4):581–611

    Article  CAS  PubMed  Google Scholar 

  11. Bagheri A, Kumar P, Kamath A, Rao P (2017) Association of angiogenic cytokines (VEGF-A and VEGF-C) and clinical characteristic in women with unexplained recurrent miscarriage. Bratisl Lek Listy 118(5):258–264

    CAS  PubMed  Google Scholar 

  12. Plaisier M, Dennert I, Rost E et al (2009) Decidual vascularization and the expression of angiogenic growth factors and proteases in first trimester spontaneous abortions. Hum Reprod 24(1):185–197

    Article  CAS  PubMed  Google Scholar 

  13. Amirchaghmaghi E, Rezaei A, Moini A et al (2015) Gene expression analysis of VEGF and its receptors and assessment of its serum level in unexplained recurrent spontaneous abortion. Cell J 16(4):538–545

    PubMed  PubMed Central  Google Scholar 

  14. Kutluer G, Cicek NM, Moraloglu O et al (2012) Low VEGF expression in conceptus material and maternal serum AFP and beta-hCG levels as indicators of defective angiogenesis in first-trimester miscarriages. J Turk Ger Gynecol Assoc 13(2):111–117

    PubMed  PubMed Central  Google Scholar 

  15. Vuorela P, Carpen O, Tulppala M, Halmesmaki E (2000) VEGF, its receptors and the tie receptors in recurrent miscarriage. Mol Hum Reprod 6(3):276–282

    Article  CAS  PubMed  Google Scholar 

  16. Christiansen OB, Nielsen HS, Kolte AM (2006) Future directions of failed implantation and recurrent miscarriage research. Reprod Biomed Online 13(1):71–83

    Article  PubMed  Google Scholar 

  17. Ben MAG, Al-Madhi SA, Zitouni H et al (2017) Vascular endothelial growth factor single nucleotide polymorphisms and haplotypes in pre-eclampsia: a case-control study. Cytokine 97:175–180

    Article  CAS  Google Scholar 

  18. Mohammadi M, Ollier WER, Hutchinson IV (2003) A functional association study of VEGF gene promoter polymorphisms with VEGF expression by stimulated pbm cells. Hum Immunol 64(10):S125–S125

    Article  Google Scholar 

  19. Almawi WY, Saldanha FL, Mahmood NA et al (2013) Relationship between VEGFA polymorphisms and serum VEGF protein levels and recurrent spontaneous miscarriage. Hum Reprod 28(10):2628–2635

    Article  CAS  PubMed  Google Scholar 

  20. Krussel J, Behr B, Hirchenhain J et al (2000) Expression of vascular endothelial growth factor mRNA in human preimplantation embryos derived from tripronuclear zygotes. Fertil Steril 74(6):1220–1226

    Article  CAS  PubMed  Google Scholar 

  21. Jung YW, Kim JO, Rah H et al (2016) Genetic variants of vascular endothelial growth factor are associated with recurrent implantation failure in Korean women. Reprod Biomed Online 32(2):190–196

    Article  CAS  PubMed  Google Scholar 

  22. Boudjenah R, Molina-Gomes D, Wainer R et al (2012) The vascular endothelial growth factor (VEGF) +405 G/C polymorphism and its relationship with recurrent implantation failure in women in an IVF programme with ICSI. J Assist Reprod Genet 29(12):1415–1420

    Article  PubMed  PubMed Central  Google Scholar 

  23. Shim SH, Kim JO, Jeon YJ et al (2018) Association between vascular endothelial growth factor promoter polymorphisms and the risk of recurrent implantation failure. Exp Ther Med 15(2):2109–2119

    CAS  PubMed  Google Scholar 

  24. Goodman C, Jeyendran RS, Coulam CB (2009) P53 tumor suppressor factor, plasminogen activator inhibitor, and vascular endothelial growth factor gene polymorphisms and recurrent implantation failure. Fertil Steril 92(2):494–498

    Article  CAS  PubMed  Google Scholar 

  25. Goodman C, Jeyendran RS, Coulam CB (2008) Vascular endothelial growth factor gene polymorphism and implantation failure. Reprod Biomed Online 16(5):720–723

    Article  CAS  PubMed  Google Scholar 

  26. Tayade C, Black GP, Fang Y, Croy BA (2006) Differential gene expression in endometrium, endometrial lymphocytes, and trophoblasts during successful and abortive embryo implantation. J Immunol 176(1):148–156

    Article  CAS  PubMed  Google Scholar 

  27. Kapiteijn K, Koolwijk P, van der Weiden RM et al (2006) Human embryo-conditioned medium stimulates in vitro endometrial angiogenesis. Fertil Steril 85(Suppl 1):1232–1239

    Article  PubMed  CAS  Google Scholar 

  28. Zeng H, He D, Xie H et al (2020) H19 regulates angiogenic capacity of extravillous trophoblasts by H19/miR-106a-5p/VEGFA axis. Arch Gynecol Obstet 301(3):671–679

    Article  CAS  PubMed  Google Scholar 

  29. Licht P, Russu V, Lehmeyer S et al (2003) Cycle dependency of intrauterine vascular endothelial growth factor levels is correlated with decidualization and corpus luteum function. Fertil Steril 80(5):1228–1233

    Article  PubMed  Google Scholar 

  30. Sugino N, Kashida S, Karube-Harada A, Takiguchi S, Kato H (2002) Expression of vascular endothelial growth factor (VEGF) and its receptors in human endometrium throughout the menstrual cycle and in early pregnancy. Reproduction 123(3):379–387

    Article  CAS  PubMed  Google Scholar 

  31. Krüssel JS, Bielfeld P, Polan ML, Simón C (2003) Regulation of embryonic implantation. Eur J Obstet Gynecol Reprod Biol 110(Suppl 1):S2-9

    Article  PubMed  CAS  Google Scholar 

  32. Dorn C, Reinsberg J, Kupka M, van der Ven H, Schild RL (2003) Leptin, VEGF, IGF-1, and IGFBP-3 concentrations in serum and follicular fluid of women undergoing in vitro fertilization. Arch Gynecol Obstet 268(3):187–193

    Article  CAS  PubMed  Google Scholar 

  33. Jinno M, Ozaki T, Iwashita M et al (2001) Measurement of endometrial tissue blood flow: a novel way to assess uterine receptivity for implantation. Fertil Steril 76(6):1168–1174

    Article  CAS  PubMed  Google Scholar 

  34. Sugino N, Kashida S, Takiguchi S, Nakamura Y, Kato H (2000) Induction of superoxide dismutase by decidualization in human endometrial stromal cells. Mol Hum Reprod 6(2):178–184

    Article  CAS  PubMed  Google Scholar 

  35. Daniel Y, Geva E, Lerner-Geva L et al (1999) Levels of vascular endothelial growth factor are elevated in patients with ectopic pregnancy: is this a novel marker? Fertil Steril 72(6):1013–1017

    Article  CAS  PubMed  Google Scholar 

  36. Fraser HM (2006) Regulation of the ovarian follicular vasculature. Reprod Biol Endocrinol 4:18

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Redmer DA, Reynolds LP (1996) Angiogenesis in the ovary. Rev Reprod 1(3):182–192

    Article  CAS  PubMed  Google Scholar 

  38. Geva E, Jaffe RB (2000) Role of vascular endothelial growth factor in ovarian physiology and pathology. Fertil Steril 74(3):429–438

    Article  CAS  PubMed  Google Scholar 

  39. Wulff C, Wilson H, Wiegand SJ, Rudge JS, Fraser HM (2002) Prevention of thecal angiogenesis, antral follicular growth, and ovulation in the primate by treatment with vascular endothelial growth factor Trap R1R2. Endocrinology 143(7):2797–2807

    Article  CAS  PubMed  Google Scholar 

  40. Redmer DA, Grazul-Bilska AT, Reynolds LP (1991) Contact-dependent intercellular communication of bovine luteal cells in culture. Endocrinology 129(5):2757–2766

    Article  CAS  PubMed  Google Scholar 

  41. Zheng J, Redmer DA, Reynolds LP (1993) Vascular development and heparin-binding growth factors in the bovine corpus luteum at several stages of the estrous cycle. Biol Reprod 49(6):1177–1189

    Article  CAS  PubMed  Google Scholar 

  42. Kamat BR, Brown LF, Manseau EJ, Senger DR, Dvorak HF (1995) Expression of vascular permeability factor/vascular endothelial growth factor by human granulosa and theca lutein cells. Role in corpus luteum development. Am J Pathol 146(1):157–165

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Brogan IJ, Khan N, Isaac K et al (1999) Novel polymorphisms in the promoter and 5’ UTR regions of the human vascular endothelial growth factor gene. Hum Immunol 60(12):1245–1249

    Article  CAS  PubMed  Google Scholar 

  44. Koukourakis MI, Papazoglou D, Giatromanolaki A et al (2004) VEGF gene sequence variation defines VEGF gene expression status and angiogenic activity in non-small cell lung cancer. Lung Cancer 46(3):293–298

    Article  PubMed  Google Scholar 

  45. Watson CJ, Webb NJ, Bottomley MJ, Brenchley PE (2000) Identification of polymorphisms within the vascular endothelial growth factor (VEGF) gene: correlation with variation in VEGF protein production. Cytokine 12(8):1232–1235

    Article  CAS  PubMed  Google Scholar 

  46. Renner W, Kotschan S, Hoffmann C, Obermayer-Pietsch B, Pilger E (2000) A common 936 C/T mutation in the gene for vascular endothelial growth factor is associated with vascular endothelial growth factor plasma levels. J Vasc Res 37(6):443–448

    Article  CAS  PubMed  Google Scholar 

  47. Tang W, Zhou T, Zhong Z, Zhong H (2019) Meta-analysis of associations of vascular endothelial growth factor protein levels and − 634G/C polymorphism with systemic lupus erythematosus susceptibility. BMC Med Genet 20(1):46

    Article  PubMed  PubMed Central  Google Scholar 

  48. Al-Habboubi HH, Sater MS, Almawi AW, Al-Khateeb GM, Almawi WY (2011) Contribution of VEGF polymorphisms to variation in VEGF serum levels in a healthy population. Eur Cytokine Netw 22(3):154–158

    Article  CAS  PubMed  Google Scholar 

  49. Lambrechts D, Storkebaum E, Morimoto M et al (2003) VEGF is a modifier of amyotrophic lateral sclerosis in mice and humans and protects motoneurons against ischemic death. Nat Genet 34(4):383–394

    Article  CAS  PubMed  Google Scholar 

  50. Shahbazi M, Fryer AA, Pravica V et al (2002) Vascular endothelial growth factor gene polymorphisms are associated with acute renal allograft rejection. J Am Soc Nephrol 13(1):260–264

    Article  CAS  PubMed  Google Scholar 

  51. Sun Y, Chen M, Mao B et al (2017) Association between vascular endothelial growth factor polymorphism and recurrent pregnancy loss: a systematic review and meta-analysis. Eur J Obstet Gynecol Reprod Biol 211:169–176

    Article  CAS  PubMed  Google Scholar 

  52. Vagnini LD, Nascimento AM, Mdo CC et al (2015) The relationship between vascular endothelial growth factor 1154G/A polymorphism and recurrent implantation failure. Med Princ Pract 24(6):533–537

    Article  PubMed  PubMed Central  Google Scholar 

  53. Stevens A, Soden J, Brenchley PE, Ralph S, Ray DW (2003) Haplotype analysis of the polymorphic human vascular endothelial growth factor gene promoter. Cancer Res 63(4):812–816

    CAS  PubMed  Google Scholar 

  54. Steffensen KD, Waldstrøm M, Brandslund I, Jakobsen A (2010) The relationship of VEGF polymorphisms with serum VEGF levels and progression-free survival in patients with epithelial ovarian cancer. Gynecol Oncol 117(1):109–116

    Article  CAS  PubMed  Google Scholar 

  55. Jung YW, Ahn EH, Kim JO et al (2018) Association of genetic polymorphisms in VEGF -460, -7 and -583 and hematocrit level with the development of idiopathic recurrent pregnancy loss and a meta-analysis. J Gene Med 20(9):e3048

    Article  PubMed  CAS  Google Scholar 

  56. Bao L, Syed R, Aloahd MS (2019) Analysis of VEGF gene polymorphisms and serum VEGF protein levels contribution in polycystic ovary syndrome of patients. Mol Biol Rep 46(6):5821–5829

    Article  CAS  PubMed  Google Scholar 

  57. Huang L, Wang L (2020) Association between VEGF gene polymorphisms (11 sites) and polycystic ovary syndrome risk. Biosci Rep 40(3).

  58. Méar L, Herr M, Fauconnier A, Pineau C, Vialard F (2020) Polymorphisms and endometriosis: a systematic review and meta-analyses. Hum Reprod Update 26(1):73–102

    Article  PubMed  CAS  Google Scholar 

  59. Bhanoori M, Babu KA, Reddy NGP et al (2005) The vascular endothelial growth factor (VEGF) +405G>C 5’-untranslated region polymorphism and increased risk of endometriosis in South Indian women: a case control study. Hum Reprod 20(7):1844–1849

    Article  CAS  PubMed  Google Scholar 

  60. Grimm C, Watrowski R, Polterauer S et al (2011) Vascular endothelial growth factor gene polymorphisms and risk of cervical intraepithelial neoplasia. Int J Gynecol Cancer 21(4):597–601

    Article  PubMed  Google Scholar 

  61. Boudjenah R, Molina-Gomes D, Torre A et al (2014) Associations between individual and combined polymorphisms of the TNF and VEGF genes and the embryo implantation rate in patients undergoing in vitro fertilization (IVF) programs. PLoS ONE 9(9):e108287

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Bányász I, Szabó S, Bokodi G et al (2006) Genetic polymorphisms of vascular endothelial growth factor in severe pre-eclampsia. Mol Hum Reprod 12(4):233–236

    Article  PubMed  CAS  Google Scholar 

  63. Altinkaya SO, Ugur M, Ceylaner G et al (2011) Vascular endothelial growth factor +405 C/G polymorphism is highly associated with an increased risk of endometriosis in Turkish women. Arch Gynecol Obstet 283(2):267–272

    Article  CAS  PubMed  Google Scholar 

  64. Kim SH, Choi YM, Choung SH et al (2005) Vascular endothelial growth factor gene +405 C/G polymorphism is associated with susceptibility to advanced stage endometriosis. Hum Reprod 20(10):2904–2908

    Article  CAS  PubMed  Google Scholar 

  65. Hanevik HI, Hilmarsen HT, Skjelbred CF, Tanbo T, Kahn JA (2012) Increased risk of ovarian hyperstimulation syndrome following controlled ovarian hyperstimulation in patients with vascular endothelial growth factor +405 cc genotype. Gynecol Endocrinol 28(11):845–849

    Article  CAS  PubMed  Google Scholar 

  66. Vanaja MC, Rozati R, Nassaruddin K, Vishnupriya S (2013) Association of VEGF +405G>C polymorphism with endometriosis. Front Biosci (Elite Ed) 5:748–754

    Article  Google Scholar 

  67. Ghasemi N, Firouzabadi RD, Ahmadi S (2017) Association of -460C/T and +405 G/C polymorphisms of vascular endothelial growth factor gene and susceptibility to ovarian hyperstimulation syndrome. Int J Reprod Biomed 15(2):87–92

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Nouri K, Haslinger P, Szabo L et al (2014) Polymorphisms of VEGF and VEGF receptors are associated with the occurrence of ovarian hyperstimulation syndrome (OHSS)-a retrospective case-control study. J Ovarian Res 7:54

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  69. Bányász I, Bokodi G, Vásárhelyi B et al (2006) Genetic polymorphisms for vascular endothelial growth factor in perinatal complications. Eur Cytokine Netw 17(4):266–270

    PubMed  Google Scholar 

  70. Li Y, Fang L, Yu Y et al (2020) Association between vascular endothelial growth factor gene polymorphisms and PCOS risk: a meta-analysis. Reprod Biomed Online 40(2):287–295

    Article  CAS  PubMed  Google Scholar 

  71. Guruvaiah P, Govatati S, Reddy TV et al (2014) The VEGF +405 G>C 5’ untranslated region polymorphism and risk of PCOS: a study in the South Indian Women. J Assist Reprod Genet 31(10):1383–1389

    Article  PubMed  PubMed Central  Google Scholar 

  72. Attar R, Agachan B, Kuran SB et al (2010) Genetic variants of vascular endothelial growth factor and risk for the development of endometriosis. Vivo 24(3):297–301

    CAS  Google Scholar 

  73. Ruggiero D, Dalmasso C, Nutile T et al (2011) Genetics of VEGF serum variation in human isolated populations of cilento: importance of VEGF polymorphisms. PLoS ONE 6(2):e16982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Yamamori M, Sakaeda T, Nakamura T et al (2004) Association of VEGF genotype with mRNA level in colorectal adenocarcinomas. Biochem Biophys Res Commun 325(1):144–150

    Article  CAS  PubMed  Google Scholar 

  75. Garza-Veloz I, Rosa C, Cortes-Flores R et al (2011) No association between polymorphisms/haplotypes of the vascular endothelial growth factor gene and preeclampsia. BMC Pregnancy Childbirth 11:35

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Wongpiyabovorn J, Hirankarn N, Ruchusatsawat K et al (2011) The association of single nucleotide polymorphism within vascular endothelial growth factor gene with systemic lupus erythematosus and lupus nephritis. Int J Immunogenet 38(1):63–67

    Article  CAS  PubMed  Google Scholar 

  77. Awata T, Inoue K, Kurihara S et al (2002) A common polymorphism in the 5’-untranslated region of the VEGF gene is associated with diabetic retinopathy in type 2 diabetes. Diabetes 51(5):1635–1639

    Article  CAS  PubMed  Google Scholar 

  78. Goldhar AS, Vonderhaar BK, Trott JF, Hovey RC (2005) Prolactin-induced expression of vascular endothelial growth factor via Egr-1. Mol Cell Endocrinol 232(1–2):9–19

    Article  CAS  PubMed  Google Scholar 

  79. Adams NR, Vasquez YM, Mo Q et al (2017) WNK lysine deficient protein kinase 1 regulates human endometrial stromal cell decidualization, proliferation, and migration in part through mitogen-activated protein kinase 7. Biol Reprod 97(3):400–412

    Article  PubMed  PubMed Central  Google Scholar 

  80. Garzia E, Borgato S, Cozzi V et al (2004) Lack of expression of endometrial prolactin in early implantation failure: a pilot study. Hum Reprod 19(8):1911–1916

    Article  CAS  PubMed  Google Scholar 

  81. Corbacho AM, Escalera GM, Clapp C (2002) Roles of prolactin and related members of the prolactin/growth hormone/placental lactogen family in angiogenesis. J Endocrinol 173(2):219–238

    Article  CAS  PubMed  Google Scholar 

  82. Li YZ, Wang LJ, Li X et al (2013) Vascular endothelial growth factor gene polymorphisms contribute to the risk of endometriosis: an updated systematic review and meta-analysis of 14 case-control studies. Genet Mol Res 12(2):1035–1044

    Article  CAS  PubMed  Google Scholar 

  83. Bhaskari J, Premalata CS, Shilpa V et al (2016) Vascular endothelial growth factor polymorphisms and a synchronized examination of plasma and tissue expression in epithelial ovarian cancers. Tumour Biol 37(1):1017–1023

    Article  CAS  PubMed  Google Scholar 

  84. Song GG, Kim JH, Lee YH (2013) Associations between vascular endothelial growth factor gene polymorphisms and pre-eclampsia susceptibility: a meta-analysis. Immunol Invest 42(8):749–762

    Article  CAS  PubMed  Google Scholar 

  85. Dong PP (2019) Association of vascular endothelial growth factor expression and polymorphisms with the risk of gestational diabetes mellitus. J Clin Lab Anal 33(2):e22686

    Article  PubMed  CAS  Google Scholar 

  86. Ikuhashi Y, Yoshida S, Kennedy S et al (2007) Vascular endothelial growth factor +936 C/T polymorphism is associated with an increased risk of endometriosis in a Japanese population. Acta Obstet Gynecol Scand 86(11):1352–1358

    Article  CAS  PubMed  Google Scholar 

  87. Henidi B, Kaabachi W, Naouali A et al (2015) Vascular endothelial growth factor (-460 C/T, +405 G/C, and +936 C/T) polymorphisms and endometriosis risk in Tunisian population. Syst Biol Reprod Med 61(4):238–244

    Article  CAS  PubMed  Google Scholar 

  88. Saboori S, Noormohammadi Z, Zare-Karizi S (2016) Genetic variation in vascular endothelial growth factor gene and its association with recurrent spontaneous abortion. Bratisl Lek Listy 117(2):80–86

    CAS  PubMed  Google Scholar 

  89. Almawi WY, Gammoh E, Malalla ZH, Al-Madhi SA (2016) Analysis of VEGFA variants and changes in VEGF levels underscores the contribution of VEGF to polycystic ovary syndrome. PLoS ONE 11(11):e0165636

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  90. Xu X, Du C, Li H et al (2015) Association of VEGF genetic polymorphisms with recurrent spontaneous abortion risk: a systematic review and meta-analysis. PLoS ONE 10(4):e0123696

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  91. Li L, Donghong L, Shuguang W et al (2013) Polymorphisms in the vascular endothelial growth factor gene associated with recurrent spontaneous miscarriage. J Matern Fetal Neonatal Med 26(7):686–690

    Article  PubMed  CAS  Google Scholar 

  92. Vagnini LD, Petersen CG, Renzi A et al (2017) A genetic test to predict recurrent implantation failure based on the association of SNPs. Hum Reprod 32:i283–i284

    Google Scholar 

  93. Bellver J, Alamá P, Gómez VH et al (2017) Recurrent implantation failure predictive capacity using an algorithm with new genetic variants associated with thrombophilia (Thrombo inCode-Implantation Failure, TiC-IF). Thromb Res 151:S129

    Google Scholar 

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Funding

This study is funded by National Key R&D Program of China (Grant Number 2018YFC1004400).

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Authors and Affiliations

  1. Foshan Maternal and Child Health Care Hospital of Southern Medical University, Foshan, 528000, Guangdong, China

    Hong Zeng & Wenmin Ma

  2. Department of Reproductive Medicine Center, NanFang Hospital of Southern Medical University, Guangzhou, 510000, Guangdong, China

    Hong Zeng & Song Quan

  3. Department of Gynecology and Obstetrics, Changsha Fourth Hospital, Changsha, 410006, China

    Lian Hu

  4. Changsha Central Hospital of Nanhua University, Changsha, 410004, Hunan, China

    Hebin Xie

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  1. Hong Zeng
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  2. Lian Hu
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  3. Hebin Xie
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  4. Wenmin Ma
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  5. Song Quan
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HZ designed the study, performed the statistical analyses, and draft the manuscript, tables and figures; HX performed the statistical analyses; LH and HX extracted the data; WM and SQ designed the study and revised the manuscript.

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Correspondence to Wenmin Ma or Song Quan.

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Zeng, H., Hu, L., Xie, H. et al. Polymorphisms of vascular endothelial growth factor and recurrent implantation failure: a systematic review and meta-analysis. Arch Gynecol Obstet 304, 297–307 (2021). https://doi.org/10.1007/s00404-021-06072-0

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