Effects of Bu-Shen-An-Tai recipe and its two components on endometrial morphology during peri-implantation in superovulated mice

Abstract

The aim of this study was to investigate the effect of Bu-Shen-An-Tai recipe (BSATR) and its two components (Bushen recipe, and Huoxue recipe) on endometrial morphology during peri-implantation in superovulated mice. Mice were randomly divided into five groups, including the normal (N), model (M), Bushen (BS), Huoxue (HX) and Bu-Shen-An-Tai (BH) groups. The uteri were collected on day 4 of pregnancy, and the endometrium thickness, microvessel density (MVD) and number of pinopodes observed. Compared with the M group, the endometrial thickness in the BS, HX and BH groups was significantly increased and there was a significant difference in endometrial thickness between the BS and the BH groups. The mean MVD was significantly lower in the M group than in the N group, and there was a significant increase in MVD in the BS, HX and BH groups as compared with the M group. Compared with the M group, the pinopode scores in the endometrium were significantly increased in the HX and BH groups; and the BS group had significantly higher pinipode scores than the HX and BH groups. In conclusion, the results of the present study demonstrated that the recipes (Bushen, Huoxue and BSATR) could improve the endometrial environment by regulating the endometrial thickness, MVD and the number of pinopodes at the window of implantation. Moreover, the Huoxue recipe and the BSATR were more efficient than the Bushen recipe, with the BSATR tending to have the most beneficial effects.

Keywords

controlled ovarian stimulation / traditional Chinese medicines / microvessel density / pinopodes / endometrium

References

[1] De los SantosM, MercaderA, GalanA, et al. . Implantation rates after two, three, or five days of embryo culture. Placenta, 2003, 24(SuppleB): S13-S19 PMID: 14559025

[2] MargaliothEJ, Ben-ChetritA, GalM, et al. . Investigation and treatment of repeated implantation failure following IVF-ET. Hum Reprod, 2006, 21(12): 3036-3043 PMID: 16905766

[3] EdwardsRG. Implantation, interception and contraception. Hum Reprod, 1994, 9(6): 985-995 PMID: 7962413

[4] Ledee-BatailleN, Lapree-DelageG, TaupinJL, et al. . Concentration of leukaemia inhibitory factor (LIF) in uterine flushing fluid is highly predictive of embryo implantation. Hum Reprod, 2002, 17(1): 213-218 PMID: 11756390

[5] PariaBC, Huet-HudsonYM, DeySK. Blastocyst’s state of activity determines the “window” of implantation in the receptive mouse uterus. Proc Natl Acad Sci USA, 1993, 90(21): 10159-10162 PMID: 8234270 PMCID: 47733

[6] CarsonDD, BagchiI, DeySK, et al. . Embryo implantation. Dev Bio, 2000, 223(2): 217-237

[7] PariaB, ReeseJ, DasSK, et al. . Deciphering the cross-talk of implantation: advances and challenges. Science, 2002, 296(5576): 2185-2188 PMID: 12077405

[8] CheckJH, ChoeJK, KatsoffD, et al. . Controlled ovarian hyperstimulation adversely affects implantation following in vitro fertilization-embryo transfer. J Assist Reprod Genet, 1999, 16(8): 416-420 PMID: 10478320 PMCID: 3455485

[9] MovagharB, AskarianS. Expression of e-cadherin, leukemia inhibitory factor and progesterone receptor in mouse blastocysts after ovarian stimulation. Cell J, 2012, 14(3): 225-230 PMID: 23508459 PMCID: 3584431

[10] BasirGS, OW S, NgEH, et al. . Morphometric analysis of peri-implantation endometrium in patients having excessively high oestradiol concentrations after ovarian stimulation. Hum Reprod, 2001, 16(3): 435-440 PMID: 11228208

[11] BourgainC, DevroeyP. The endometrium in stimulated cycles for IVF. Hum Reprod Update, 2003, 9(6): 515-522 PMID: 14714588

[12] ErtzeidG, StorengR. The impact of ovarian stimulation on implantation and fetal development in mice. Hum Reprod, 2001, 16(2): 221-225 PMID: 11157810

[13] CarloneDL, RiderV. Embryonic modulation of basic fibroblast growth factor in the rat uterus. Biol Reprod, 1993, 49(4): 653-665 PMID: 8218629

[14] Charnock-JonesDS, KaufmannP, MayhewTM. Aspects of human fetoplacental vasculogenesis and angiogenesis. I. Molecular regulation. Placenta, 2004, 25(2–3): 103-113 PMID: 14972443

[15] Red-HorseK, DrakePM, FisherSJ. Human pregnancy: the role of chemokine networks at the fetal-maternal interface. Expert Rev Mol Med, 2004, 6(11): 1-14 PMID: 15130179

[16] DengSR, LiJ, ZhangZQ, et al. . DS147 improves pregnancy in mice with embryo implantation dysfunction induced by controlled ovarian stimulation. J Huazhong Univer Scid Technol [Med Sci], 2013, 33(4): 573-580

[17] NardoLG, SabatiniL, RaiR, et al. . Pinopode expression during human implantation. Eur J Obstet Gynecol Reprod Biol, 2002, 101(2): 104-108 PMID: 11858881

[18] NikasG. Pinopodes as markers of endometrial receptivity in clinical practice. Hum Reprod, 1999, 14(Suppl2): 99-106 PMID: 10690805

[19] NikasG, DeveliogluOH, TonerJP, et al. . Endometrial pinopodes indicate a shift in the window of receptivity in IVF cycles. Hum Reprod, 1999, 14(3): 787-792 PMID: 10221715

[20] NikasG, MakrigiannakisA. Endometrial pinopodes and uterine receptivity. Ann N Y Acad Sci, 2003, 997: 120-123 PMID: 14644817

[21] NilssonO. Ultrastructure of mouse uterine surface epithelium under different estrogenic influences. 2. Early effect of estrogen administered to spayed animals. J Ultrastruct Res, 1958, 2(1): 73-95 PMID: 13631742

[22] JohannissonE, NilssonL. Scanning electron microscopic study of the human endometrium. Fertil Steril, 1972, 23(9): 613-625 PMID: 5050292

[23] MartelD, FrydmanR, GlissantM, et al. . Scanning electron microscopy of postovulatory human endometrium in spontaneous cycles and cycles stimulated by hormone treatment. J Endocrinol, 1987, 114(2): 319-24 PMID: 3116141

[24] Bentin-LeyU, SjogrenA, NilssonL, et al. . Presence of uterine pinopodes at the embryo-endometrial interface during human implantation in vitro. Hum Reprod, 1999, 14(2): 515-520 PMID: 10100003

[25] AplinJ D. Embryo implantation: the molecular mechanism remains elusive. Reprod Biomed Online, 2006, 13(6): 833-839 PMID: 17169205

[26] Kabir-SalmaniM, NikzadH, ShiokawaS, et al. . Secretory role for human uterodomes (pinopods): secretion of LIF. Mol Hum Reprod, 2005, 11(8): 553-559 PMID: 16126773

[27] Stavreus-EversA, AghajanovaL, BrismarH, et al. . Co-existence of heparin-binding epidermal growth factor-like growth factor and pinopodes in human endometrium at the time of implantation. Mol Hum Reprod, 2002, 8(8): 765-769 PMID: 12149409

[28] NikasG, AghajanovaL. Endometrial pinopodes: some more understanding on human implantation?. Reprod Biomed Online, 2002, 4(Suppl3): 18-23 PMID: 12470560

[29] AlbertsonK. The use of traditional Chinese medicine for treating female infertility, 2006, Birmingham, AL, Clayton College of Natural Health

[30] AlfredA, RiedK. Traditional Chinese medicine—women’s experiences in the treatment of infertility. Aust Fam Physician, 2011, 40(9): 718-722 PMID: 21894282

[31] LewisR. The infertility cure: the ancient Chinese wellness program for getting pregnant and having healthy babies, 2008

[32] MaciociaG, LivingstoneC. Obstetrics & gynecology in Chinese medicine, 1998

[33] NollA A, WilmsS. Chinese medicine in fertility disorders, 2009

[34] RiedK, StuartK. Efficacy of traditional Chinese herbal medicine in the management of female infertility: a systematic review. Complement Ther Med, 2011, 19(6): 319-331 PMID: 22036524

[35] JiaY, MengY, ZhangM. Comparative study of bushenantai recipe and its two components on blastocyst implantation of controlled ovarian hyperstimulation. Zhongxiyi Jiehe Yanjin (Chinese), 2010, 2(6): 288-293

[36] WeidnerN. Current pathologic methods for measuring intratumoral microvessel density within breast carcinoma and other solid tumors. Breast Cancer Res Treat, 1995, 36(2): 169-180 PMID: 8534865

[37] UsadiRS, MurrayMJ, BagnellRC, et al. . Temporal and morphologic characteristics of pinopod expression across the secretory phase of the endometrial cycle in normally cycling women with proven fertility. Fertil Steril, 2003, 79(4): 970-974 PMID: 12749439

[38] WangH, DeySK. Roadmap to embryo implantation: clues from mouse models. Nat Rev Genet, 2006, 7(3): 185-199 PMID: 16485018

[39] MurrayMJ, MeyerWR, ZainoR J, et al. . A critical analysis of the accuracy, reproducibility, and clinical utility of histologic endometrial dating in fertile women. Fertil Steril, 2004, 81(5): 1333-1343 PMID: 15136099

[40] ZhangX, ChenCH, ConfinoE, et al. . Increased endometrial thickness is associated with improved treatment outcome for selected patients undergoing in vitro fertilization-embryo transfer. Fertil Steril, 2005, 83(2): 336-340 PMID: 15705371

[41] AbdallaH, BrooksA, JohnsonM, et al. . Endometrial thickness: a predictor of implantation in ovum recipients?. Human Reproduction, 1994, 9(2): 363-365 PMID: 8027298

[42] NoyesN, LiuHC, SultanK, et al. . Implantation: Endometrial thickness appears to be a significant factor in embryo implantation in in-vitro fertilization. Hum Reprod, 1995, 10(4): 919-922 PMID: 7650143

[43] BarkerD. Developmental origins of adult health and disease. J Epidemiol Community Health, 2004, 58(2): 114 PMID: 14729887 PMCID: 1732687

[44] NorwitzER. Defective implantation and placentation: laying the blueprint for pregnancy complications. Reprod Biomed Online, 2007, 14(1): 101-109 PMID: 20483405

[45] TianwenX, DaodaC. Serum vascular endothelial growth factor-C and vascular endothelial growth factor level in patients with colorectal carcinoma and clinical significance. J Huazhong Univer Sci Technol [Med Sci], 2006, 26(3): 329-331

[46] ChenW, LuY, WuJ, et al. . Beta-elemene inhibits melanoma growth and metastasis via suppressing vascular endothelial growth factor-mediated angiogenesis. Cancer Chemother Pharmacol, 2011, 67(4): 799-808 PMID: 20563582

[47] DeyS, LimH, DasS K, et al. . Molecular cues to implantation. Endocr Rev, 2004, 25(3): 341-373 PMID: 15180948

[48] KolbBA, NajmabadiS, PaulsonRJ. Ultrastructural characteristics of the luteal phase endometrium in patients undergoing controlled ovarian hyperstimulation. Fertil Steril, 1997, 67(4): 625-630 PMID: 9093184

[49] DeveliogluOH, HsiuJG, NikasG, et al. . Endometrial estrogen and progesterone receptor and pinopode expression in stimulated cycles of oocyte donors. Fertil Steril, 1999, 71(6): 1040-1047 PMID: 10360907

[50] WangL, ZhouGB, LiuP, et al. . Dissection of mechanisms of Chinese medicinal formula Realgar-Indigo naturalis as an effective treatment for promyelocytic leukemia. Proc Natl Acad Sci USA, 2008, 105(12): 4826-4831 PMID: 18344322 PMCID: 2290784