Application of Growth Hormone in in vitro Fertilization

Yue-Ming Xu, Gui-Min Hao, Bu-Lang Gao, Yue-Ming Xu, Gui-Min Hao, Bu-Lang Gao

Abstract

Growth hormone (GH) is a peptide hormone secreted mainly by the anterior part of the pituitary gland and plays a critical role in cell growth, development, and metabolism throughout the body. GH can not only directly influence human oocytes and cumulus cells but also indirectly improve oocyte quality through activating synthesis of insulin-like growth factor-I or promoting follicle-stimulating hormone-induced ovarian steroidogenesis. Since GH can regulate female and male infertility, it has been applied in the management of infertility for many years, especially in patients with poor ovarian response or poor prognosis. During ovarian stimulation, GH administration might improve the success rate of in vitro fertilization (IVF) probably through the beneficial effects of GH on oocyte quality as indicated by a higher number of mature oocytes and embryos arriving at the transfer stage and a higher fertility rate in GH-treated patients. However, there is still great controversy in the application of GH in IVF. While some researchers showed that pregnancy, implantation and live birth rates could be increased by ovarian pretreatment with GH, others did not support GH as an effective adjuvant for infertility treatment because the live birth rate was not increased. This study reviewed and summarized recent advancements and benefits in clinical application of GH, trying to reach a just unbiased conclusion regarding the effect of GH therapy in IVF.

Keywords: effect; growth hormone; in vitro fertilization; infertility; reproduction.

Figures

Figure 1
Figure 1
Growth hormone (GH) acts through some signal pathways. ERK, extracellular signal-regulated kinase; GHR, growth hormone receptor; Grb, growth factor receptor-bound protein; IRS, insulin receptor substrate; IGF 1, insulin-like growth factor 1; JAK2, Janus kinase 2; MAPK, mitogen-activated protein kinase; MEK, dual specificity mitogen-activated protein kinase 2; PI3K, phosphatidyl inositol 3 kinase; SHC, SH2-domain containing transforming protein; SIRP, signal regulatory protein; SOS, son of sevenless; STAT, signal transducer and activator of transcription.

References

    1. Altmae S, Mendoza-Tesarik R, Mendoza C, Mendoza N, Cucinelli F, Tesarik J. Effect of growth hormone on uterine receptivity in women with repeated implantation failure in an oocyte donation program: a randomized controlled trial. J Endocr Soc. (2018) 2:96–105. 10.1210/js.2017-00359
    1. Abir R, Garor R, Felz C, Nitke S, Krissi H, Fisch B. Growth hormone and its receptor in human ovaries from fetuses and adults. Fertil Steril. (2008) 90:1333–9. 10.1016/j.fertnstert.2007.08.011
    1. Menezo YJ, el Mouatassim S, Chavrier M, Servy EJ, Nicolet B. Human oocytes and preimplantation embryos express mRNA for growth hormone receptor. Zygote. (2003) 11:293–7. 10.1017/S096719940300234X
    1. Menezo YJ, Nicollet B, Rollet J, Hazout A. Pregnancy and delivery after in vitro maturation of naked iCSI-gV oocytes with GH and transfer of a frozen thawed blastocyst: case report. J Assist Reprod Genet. (2006) 23:47–9. 10.1007/s10815-005-9014-0
    1. Cui N, Li AM, Luo ZY, Zhao ZM, Xu YM, Zhang J, et al. Effects of growth hormone on pregnancy rates of patients with thin endometrium. J Endocrinol Invest. (2019) 42:27–35. 10.1007/s40618-018-0877-1
    1. Hull KL, Harvey S. Growth hormone and reproduction: a review of endocrine and autocrine/paracrine interactions. Int j endocrinol. (2014) 2014:234014. 10.1155/2014/234014
    1. Magon N, Agrawal S, Malik S, Babu KM. Growth hormone in the management of female infertility. Indian J Endocrinol Metab. (2011) 15 (Suppl. 3):S246–7. 10.4103/2230-8210.84876
    1. Bassiouny YA, Dakhly DMR, Bayoumi YA, Hashish NM. Does the addition of growth hormone to the in vitro fertilization/intracytoplasmic sperm injection antagonist protocol improve outcomes in poor responders? a randomized, controlled trial. Fertil Steril. (2016) 105:697–702. 10.1016/j.fertnstert.2015.11.026
    1. Duffy JM, Ahmad G, Mohiyiddeen L, Nardo LG, Watson A. Growth hormone for in vitro fertilization. Cochrane Database Syst Rev. (2010) CD000099. 10.1002/14651858.CD000099.pub3
    1. Kolibianakis EM, Venetis CA, Diedrich K, Tarlatzis BC, Griesinger G. Addition of growth hormone to gonadotrophins in ovarian stimulation of poor responders treated by in-vitro fertilization: a systematic review and meta-analysis. Hum Reprod Update. (2009) 15:613–22. 10.1093/humupd/dmp026
    1. Li XL, Wang L, Lv F, Huang XM, Wang LP, Pan Y, et al. . The influence of different growth hormone addition protocols to poor ovarian responders on clinical outcomes in controlled ovary stimulation cycles: a systematic review and meta-analysis. Medicine. (2017) 96:e6443. 10.1097/MD.0000000000006443
    1. Du XF, Yang XH, Li J, Hao M, Guo YH. Growth hormone co-treatment within a GnRH agonist long protocol improves implantation and pregnancy rates in patients undergoing IVF-eT. Arch Gynecol Obstet. (2016) 294:877–83. 10.1007/s00404-016-4163-1
    1. Tesarik J, Hazout A, Mendoza C. Improvement of delivery and live birth rates after iCSI in women aged >40 years by ovarian co-stimulation with growth hormone. Hum Reprod. (2005) 20:2536–41. 10.1093/humrep/dei066
    1. Kucuk T, Kozinoglu H, Kaba A. Growth hormone co-treatment within a gnRH agonist long protocol in patients with poor ovarian response: a prospective, randomized, clinical trial. J Assist Reprod Genet. (2008) 25:123–7. 10.1007/s10815-008-9212-7
    1. Hazout A, Junca A, Menezo Y, Demouzon J, Cohen-Bacrie P. Effect of growth hormone on oocyte competence in patients with multiple IVF failures. Reprod Biomed Online. (2009) 18:664–70. 10.1016/S1472-6483(10)60011-9
    1. Lattes K, Brassesco M, Gomez M, Checa MA. Low-dose growth hormone supplementation increases clinical pregnancy rate in poor responders undergoing in vitro fertilisation. Gynecol Endocrinol. (2015) 31:565–8. 10.3109/09513590.2015.1025378
    1. Yovich JL, Stanger JD. Growth hormone supplementation improves implantation and pregnancy productivity rates for poor-prognosis patients undertaking IVF. Reprod Biomed Online. (2010) 21:37–49. 10.1016/j.rbmo.2010.03.013
    1. Dakhly DMR, Bassiouny YA, Bayoumi YA, Hassan MA, Gouda HM, Hassan AA. The addition of growth hormone adjuvant therapy to the long down regulation protocol in poor responders undergoing in vitro fertilization: randomized control trial. Eur J Obstet Gynecol Reprod Biol. (2018) 228:161–5. 10.1016/j.ejogrb.2018.06.035
    1. Norman RJ, Alvino H, Hull LM, Mol BW, Hart RJ, Kelly TL, et al. . Human growth hormone for poor responders: a randomized placebo-controlled trial provides no evidence for improved live birth rate. Reprod Biomed Online. (2019) 38:908–15. 10.1016/j.rbmo.2019.02.003
    1. Yovich JL, Ye Y, Keane KN. Growth hormone adjuvant trial for poor responders undergoing IVF. Eur J Obstet Gynecol Reprod Biol. (2019) 236:249. 10.1016/j.ejogrb.2019.01.026
    1. de Boer JA, Schoemaker J, van der Veen EA. Impaired reproductive function in women treated for growth hormone deficiency during childhood. Clin Endocrinol. (1997) 46:681–9. 10.1046/j.1365-2265.1997.1800999.x
    1. Giampietro A, Milardi D, Bianchi A, Fusco A, Cimino V, Valle D, et al. . The effect of treatment with growth hormone on fertility outcome in eugonadal women with growth hormone deficiency: report of four cases and review of the literature. Fertil Steril. (2009) 91:930.e7–11. 10.1016/j.fertnstert.2008.09.065
    1. Sirotkin AV. Control of reproductive processes by growth hormone: extra- and intracellular mechanisms. Vet J. (2005) 170:307–17. 10.1016/j.tvjl.2004.05.014
    1. Brunet-Dunand SE, Vouyovitch C, Araneda S, Pandey V, Vidal LJ, Print C, et al. . Autocrine human growth hormone promotes tumor angiogenesis in mammary carcinoma. Endocrinology. (2009) 150:1341–52. 10.1210/en.2008-0608
    1. Wajnrajch MP. Physiological and pathological growth hormone secretion. J Pediatr Endocrinol Metab. (2005) 18:325–38. 10.1515/JPEM.2005.18.4.325
    1. van den Eijnden MJ, Strous GJ. Autocrine growth hormone: effects on growth hormone receptor trafficking and signaling. Mol Endocrinol. (2007) 21:2832–46. 10.1210/me.2007-0092
    1. Carter-Su C, Schwartz J, Argetsinger LS. Growth hormone signaling pathways. Growth Horm IGF Res. (2016) 28:11–5. 10.1016/j.ghir.2015.09.002
    1. VanderKuur J, Allevato G, Billestrup N, Norstedt G, Carter-Su C. Growth hormone-promoted tyrosyl phosphorylation of SHC proteins and SHC association with grb2. J Biol Chem. (1995) 270:7587–93. 10.1074/jbc.270.13.7587
    1. Vanderkuur JA, Butch ER, Waters SB, Pessin JE, Guan KL, Carter-Su C. Signaling molecules involved in coupling growth hormone receptor to mitogen-activated protein kinase activation. Endocrinology. (1997) 138:4301–7. 10.1210/endo.138.10.5453
    1. Zehorai E, Yao Z, Plotnikov A, Seger R. The subcellular localization of MEK and ERK–a novel nuclear translocation signal (NTS) paves a way to the nucleus. Mol Cell Endocrinol. (2010) 314:213–20. 10.1016/j.mce.2009.04.008
    1. Adamson U. On the diabetogenic effect of growth hormone in man: effects of growth hormone of glucagon and insulin secretion. Eur J Clin Invest. (1981) 11:115–9. 10.1111/j.1365-2362.1981.tb02048.x
    1. Argetsinger LS, Hsu GW, Myers MG, Jr, Billestrup N, White MF, Carter-Su C. Growth hormone, interferon-gamma, and leukemia inhibitory factor promoted tyrosyl phosphorylation of insulin receptor substrate-1. J Biol Chem. (1995) 270:14685–92. 10.1074/jbc.270.24.14685
    1. Argetsinger LS, Norstedt G, Billestrup N, White MF, Carter-Su C. Growth hormone, interferon-gamma, and leukemia inhibitory factor utilize insulin receptor substrate-2 in intracellular signaling. J Biol Chem. (1996) 271:29415–21. 10.1074/jbc.271.46.29415
    1. Alessi DR, James SR, Downes CP, Holmes AB, Gaffney PR, Reese CB, et al. . Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase balpha. Curr Biol. (1997) 7:261–9. 10.1016/S0960-9822(06)00122-9
    1. Piwien-Pilipuk G, Van Mater D, Ross SE, MacDougald OA, Schwartz J. Growth hormone regulates phosphorylation and function of cCAAT/enhancer-binding protein beta by modulating akt and glycogen synthase kinase-3. J Biol Chem. (2001) 276:19664–71. 10.1074/jbc.M010193200
    1. Campbell GS, Meyer DJ, Raz R, Levy DE, Schwartz J, Carter-Su C. Activation of acute phase response factor (aPRF)/stat3 transcription factor by growth hormone. J Biol Chem. (1995) 270:3974–9. 10.1074/jbc.270.8.3974
    1. Meyer DJ, Campbell GS, Cochran BH, Argetsinger LS, Larner AC, Finbloom DS, et al. . Growth hormone induces a DNA binding factor related to the interferon-stimulated 91-kDa transcription factor. J Biol Chem. (1994) 269:4701–4.
    1. Sotiropoulos A, Moutoussamy S, Renaudie F, Clauss M, Kayser C, Gouilleux F, et al. . Differential activation of stat3 and stat5 by distinct regions of the growth hormone receptor. Mol Endocrinol. (1996) 10:998–1009. 10.1210/mend.10.8.8843416
    1. Singh AK, Lal B. Seasonal and circadian time-dependent dual action of GH on somatic growth and ovarian development in the asian catfish, clarias batrachus (linn.): role of temperature. Gen Comp Endocrinol. (2008) 159:98–106. 10.1016/j.ygcen.2008.08.001
    1. Arunakumari G, Shanmugasundaram N, Rao VH. Development of morulae from the oocytes of cultured sheep preantral follicles. Theriogenology. (2010) 74:884–94. 10.1016/j.theriogenology.2010.04.013
    1. Liu X, Andoh K, Yokota H, Kobayashi J, Abe Y, Yamada K, et al. . Effects of growth hormone, activin, and follistatin on the development of preantral follicle from immature female mice. Endocrinology. (1998) 139:2342–7. 10.1210/endo.139.5.5987
    1. Magalhaes DM, Duarte AB, Araujo VR, Brito IR, Soares TG, Lima IM, et al. . In vitro production of a caprine embryo from a preantral follicle cultured in media supplemented with growth hormone. Theriogenology. (2011) 75:182–8. 10.1016/j.theriogenology.2010.08.004
    1. Kobayashi J, Mizunuma H, Kikuchi N, Liu X, Andoh K, Abe Y, et al. . Morphological assessment of the effect of growth hormone on preantral follicles from 11-day-old mice in an in vitro culture system. Biochem Biophys Res Commun. (2000) 268:36–41. 10.1006/bbrc.1999.2072
    1. Hassan HA, Azab H, Rahman AA, Nafee TM. Effects of growth hormone on in vitro maturation of germinal vesicle of human oocytes retrieved from small antral follicles. J Assist Reprod Genet. (2001) 18:417–20. 10.1023/A:1016630603560
    1. de Prada JK, VandeVoort CA. Growth hormone and in vitro maturation of rhesus macaque oocytes and subsequent embryo development. J Assist Reprod Genet. (2008) 25:145–58. 10.1007/s10815-008-9208-3
    1. Gonzalez-Anover P, Encinas T, Garcia-Garcia RM, Veiga-Lopez A, Cocero MJ, McNeilly AS, et al. . Ovarian response in sheep superovulated after pretreatment with growth hormone and gnRH antagonists is weakened by failures in oocyte maturation. Zygote. (2004) 12:301–4. 10.1017/S096719940400293X
    1. Sa Filho MF, Carvalho NA, Gimenes LU, Torres-Junior JR, Nasser LF, Tonhati H, et al. . Effect of recombinant bovine somatotropin (bST) on follicular population and on in vitro buffalo embryo production. Anim Reprod Sci. (2009) 113:51–9. 10.1016/j.anireprosci.2008.06.008
    1. Semiz O, Evirgen O. The effect of growth hormone on ovarian follicular response and oocyte nuclear maturation in young and aged mice. Acta Histochem. (2009) 111:104–11. 10.1016/j.acthis.2008.04.007
    1. Hrabia A, Sechman A, Gertler A, Rzasa J. Effect of growth hormone on steroid content, proliferation and apoptosis in the chicken ovary during sexual maturation. Cell Tissue Res. (2011) 345:191–202. 10.1007/s00441-011-1187-5
    1. Flores R, Looper ML, Rorie RW, Hallford DM, Rosenkrans CF, Jr. Endocrine factors and ovarian follicles are influenced by body condition and somatotropin in postpartum beef cows. J Anim Sci. (2008) 86:1335–44. 10.2527/jas.2007-0574
    1. Adams NR, Briegel JR. Multiple effects of an additional growth hormone gene in adult sheep. J Anim Sci. (2005) 83:1868–74. 10.2527/2005.8381868x
    1. Cecim M, Kerr J, Bartke A. Effects of bovine growth hormone (bGH) transgene expression or bGH treatment on reproductive functions in female mice. Biol Reprod. (1995) 52:1144–8. 10.1095/biolreprod52.5.1144
    1. Martins FS, Saraiva MV, Magalhaes-Padilha DM, Almeida AP, Celestino JJ, Padilha RT, et al. . Presence of growth hormone receptor (GH-r) mRNA and protein in goat ovarian follicles and improvement of in vitro preantral follicle survival and development with GH. Theriogenology. (2014) 82:27–35. 10.1016/j.theriogenology.2014.02.019
    1. Weall BM, Al-Samerria S, Conceicao J, Yovich JL, Almahbobi G. A direct action for GH in improvement of oocyte quality in poor-responder patients. Reproduction. (2015) 149:147–54. 10.1530/REP-14-0494
    1. Levi AJ, Drews MR, Bergh PA, Miller BT, Scott RT., Jr Controlled ovarian hyperstimulation does not adversely affect endometrial receptivity in in vitro fertilization cycles. Fertil Steril. (2001) 76:670–4. 10.1016/S0015-0282(01)01988-4
    1. Xue-Mei W, Hong J, Wen-Xiang Z, Yang L. The effects of growth hormone on clinical outcomes after frozen-thawed embryo transfer. Int J Gynaecol Obstet. (2016) 133:347–50. 10.1016/j.ijgo.2015.10.020
    1. Momeni M, Rahbar MH, Kovanci E. A meta-analysis of the relationship between endometrial thickness and outcome of in vitro fertilization cycles. J Hum Reprod Sci. (2011) 4:130–7. 10.4103/0974-1208.92287
    1. Homburg R, Eshel A, Abdalla HI, Jacobs HS. Growth hormone facilitates ovulation induction by gonadotrophins. Clin Endocrinol. (1988) 29:113–7. 10.1111/j.1365-2265.1988.tb00252.x
    1. Owen EJ, West C, Mason BA, Jacobs HS. Co-treatment with growth hormone of sub-optimal responders in IVF-eT. Hum Reprod. (1991) 6:524–8. 10.1093/oxfordjournals.humrep.a137372
    1. de Ziegler D, Streuli I, Meldrum DR, Chapron C. The value of growth hormone supplements in art for poor ovarian responders. Fertil Steril. (2011) 96:1069–76. 10.1016/j.fertnstert.2011.09.049
    1. Chu K, Pang W, Sun N, Zhang Q, Li W. Outcomes of poor responders following growth hormone co-treatment with IVF/iCSI mild stimulation protocol: a retrospective cohort study. Arch Gynecol Obstet. (2018) 297:1317–21. 10.1007/s00404-018-4725-5
    1. Dunne C, Seethram K, Roberts J. Growth hormone supplementation in the luteal phase before microdose gnrh agonist flare protocol for in vitro fertilization. J Obstet Gynaecol Can. (2015) 37:810–5. 10.1016/S1701-2163(15)30152-3
    1. Ho YK, Lee TH, Lee CI, Cheng EH, Huang CC, Huang LS, et al. . Effects of growth hormone plus gonadotropins on controlled ovarian stimulation in infertile women of advanced age, poor responders, and previous in vitro fertilization failure patients. Taiwan J Obstet Gynecol. (2017) 56:806–10. 10.1016/j.tjog.2017.10.018
    1. Regan SLP, Knight PG, Yovich JL, Arfuso F, Dharmarajan A. Growth hormone during in vitro fertilization in older women modulates the density of receptors in granulosa cells, with improved pregnancy outcomes. Fertil Steril. (2018) 110:1298–310. 10.1016/j.fertnstert.2018.08.018
    1. Hart RJ, Rombauts L, Norman RJ. Growth hormone in IVF cycles: any hope? Curr Opin Obstet Gynecol. (2017) 29:119–25. 10.1097/GCO.0000000000000360
    1. Kotarba D, Kotarba J, Hughes E. Growth hormone for in vitro fertilization. Cochrane Database Syst Rev. (2000) CD000099. 10.1002/14651858.CD000099
    1. Yu X, Ruan J, He LP, Hu W, Xu Q, Tang J, et al. . Efficacy of growth hormone supplementation with gonadotrophins in vitro fertilization for poor ovarian responders: an updated meta-analysis. Int J Clin Exp Med. (2015) 8:4954–67.
    1. Kyrou D, Kolibianakis EM, Venetis CA, Papanikolaou EG, Bontis J, Tarlatzis BC. How to improve the probability of pregnancy in poor responders undergoing in vitro fertilization: a systematic review and meta-analysis. Fertil Steril. (2009) 91:749–66. 10.1016/j.fertnstert.2007.12.077
    1. Bayoumi YA, Dakhly DM, Bassiouny YA, Hashish NM. Addition of growth hormone to the microflare stimulation protocol among women with poor ovarian response. Int J Gynaecol Obstet. (2015) 131:305–8. 10.1016/j.ijgo.2015.05.034
    1. Cai MH, Liang XY, Wu YQ, Huang R, Yang X. Six-week pretreatment with growth hormone improves clinical outcomes of poor ovarian responders undergoing in vitro fertilization treatment: a self-controlled clinical study. J Obstet Gynaecol Res. (2019) 45:376–81. 10.1111/jog.13823
    1. Choe SA, Kim MJ, Lee HJ, Kim J, Chang EM, Kim JW, et al. . Increased proportion of mature oocytes with sustained-release growth hormone treatment in poor responders: a prospective randomized controlled study. Arch Gynecol Obstet. (2018) 297:791–6. 10.1007/s00404-017-4613-4
    1. Eftekhar M, Aflatoonian A, Mohammadian F, Eftekhar T. Adjuvant growth hormone therapy in antagonist protocol in poor responders undergoing assisted reproductive technology. Arch Gynecol Obstet. (2013) 287:1017–21. 10.1007/s00404-012-2655-1
    1. Guan Q, Ma HG, Wang YY, Zhang F. [effects of co-administration of growth hormone(GH) and aspirin to women during in vitro fertilization and embryo transfer (IVF-eT) cycles]. Zhonghua Nan Ke Xue. (2007) 13:798–800.
    1. Ob'edkova K, Kogan I, Krikheli I, Dzhemlikhanova L, Muller V, Mekina I, et al. . Growth hormone co-treatment in IVF/iCSI cycles in poor responders. Gynecol Endocrinol. (2017) 33:15–7. 10.1080/09513590.2017.1399693
    1. Santibanez-Morales A, Duran-Boullosa E, Colin-Licea EO. [Use of growth hormone for in vitro fertilization]. Ginecol Obstet Mex. (2016) 84:567–72.
    1. Sugaya S, Suzuki M, Fujita K, Kurabayashi T, Tanaka K. Effect of cotreatment with growth hormone on ovarian stimulation in poor responders to in vitro fertilization. Fertil Steril. (2003) 79:1251–3. 10.1016/S0015-0282(02)04959-2
    1. Keane KN, Yovich JL, Hamidi A, Hinchliffe PM, Dhaliwal SS. Single-centre retrospective analysis of growth hormone supplementation in IVF patients classified as poor-prognosis. BMJ Open. (2017) 7:e018107. 10.1136/bmjopen-2017-018107
    1. Drakopoulos P, Pluchino N, Bischof P, Cantero P, Meyer P, Chardonnens D. Effect of growth hormone on endometrial thickness and fertility outcome in the treatment of women with panhypopituitarism: a case report. J Reprod Med. (2016) 61:78–82.
    1. Liu X, Bai H, Xie J, Shi J. Growth hormone co-treatment on controlled ovarian stimulation in normal ovarian response women can improve embryo quality. Gynecol Endocrinol. (2019) 23:1–5. 10.1080/09513590.2019.1590545
    1. Arefi S, Hoseini A, Farifteh F, Zeraati H. Modified natural cycle frozen-thawed embryo transfer in patients with repeated implantation failure: an observational study. Int J Reprod Biomed. (2016) 14:465–70. 10.29252/ijrm.14.7.5
    1. Chen Y, Liu F, Nong Y, Ruan J, Guo Q, Luo M, et al. . Clinical efficacy and mechanism of growth hormone action in patients experiencing repeat implantation failure. Can J Physiol Pharmacol. (2018) 96:929–32. 10.1139/cjpp-2017-0786
    1. Rahman A, Francomano D, Sagnella F, Lisi F, Manna C. The effect on clinical results of adding recombinant LH in late phase of ovarian stimulation of patients with repeated implantation failure: a pilot study. Eur Rev Med Pharmacol Sci. (2017) 21:5485–90. 10.26355/eurrev_201712_13939
    1. Dakhly DM, Bayoumi YA, Gad Allah SH. Which is the best IVF/iCSI protocol to be used in poor responders receiving growth hormone as an adjuvant treatment? a prospective randomized trial. Gynecol Endocrinol. (2016) 32:116–9. 10.3109/09513590.2015.1092136
    1. Otsuka F, McTavish KJ, Shimasaki S. Integral role of GDF-9 and BMP-15 in ovarian function. Mol Reprod Dev. (2011) 78:9–21. 10.1002/mrd.21265
    1. Abdalla HI, Brooks AA, Johnson MR, Kirkland A, Thomas A, Studd JW. Endometrial thickness: a predictor of implantation in ovum recipients? Hum Reprod. (1994) 9:363–5. 10.1093/oxfordjournals.humrep.a138509
    1. Miwa I, Tamura H, Takasaki A, Yamagata Y, Shimamura K, Sugino N. Pathophysiologic features of “thin” endometrium. Fertil steril. (2009) 91:998–1004. 10.1016/j.fertnstert.2008.01.029
    1. Richter KS, Bugge KR, Bromer JG, Levy MJ. Relationship between endometrial thickness and embryo implantation, based on 1,294 cycles of in vitro fertilization with transfer of two blastocyst-stage embryos. Fertil steril. (2007) 87:53–9. 10.1016/j.fertnstert.2006.05.064
    1. Smith SK. Angiogenesis, vascular endothelial growth factor and the endometrium. Hum Reprod Update. (1998) 4:509–19. 10.1093/humupd/4.5.509
    1. Smith SK. Angiogenesis and implantation. Hum Reprod. (2000) 15(Suppl. 6):59–66.
    1. Hurst BS, Bhojwani JT, Marshburn PB, Papadakis MA, Loeb TA, Matthews ML. Low-dose aspirin does not improve ovarian stimulation, endometrial response, or pregnancy rates for in vitro fertilization. J Exp Clin Assist Reprod. (2005) 2:8 10.1186/1743-1050-2-8
    1. Sher G, Fisch JD. Effect of vaginal sildenafil on the outcome of in vitro fertilization (IVF) after multiple IVF failures attributed to poor endometrial development. Fertil steril. (2002) 78:1073–6. 10.1016/S0015-0282(02)03375-7
    1. Chien LW, Au HK, Chen PL, Xiao J, Tzeng CR. Assessment of uterine receptivity by the endometrial-subendometrial blood flow distribution pattern in women undergoing in vitro fertilization-embryo transfer. Fertil steril. (2002) 78:245–51. 10.1016/S0015-0282(02)03223-5
    1. Friedler S, Schenker JG, Herman A, Lewin A. The role of ultrasonography in the evaluation of endometrial receptivity following assisted reproductive treatments: a critical review. Hum Reprod Update. (1996) 2:323–35. 10.1093/humupd/2.4.323
    1. Kaneko Y, Day ML, Murphy CR. Integrin beta3 in rat blastocysts and epithelial cells is essential for implantation in vitro: studies with ishikawa cells and small interfering RNA transfection. Hum reprod. (2011) 26:1665–74. 10.1093/humrep/der128
    1. Lessey BA, Castelbaum AJ. Integrins and implantation in the human. Rev endocr metab disord. (2002) 3:107–17. 10.1023/A:1015450727580
    1. Tei C, Maruyama T, Kuji N, Miyazaki T, Mikami M, Yoshimura Y. Reduced expression of alphavbeta3 integrin in the endometrium of unexplained infertility patients with recurrent IVF-eT failures: improvement by danazol treatment. J assist reprod genet. (2003) 20:13–20. 10.1023/A:1021254620888
    1. Wu HB, Li MJ, Luo JX. Application of growth hormone to the poor ovarian responders during in vitro fertilization and embryo transfer antagonist protocol. Chin Reprod Contracept. (2016) 36:416–20.
    1. Khalid M, Haresign W, Luck MR. Secretion of IGF-1 by ovine granulosa cells: effects of growth hormone and follicle stimulating hormone. Anim Reprod Sci. (2000) 58:261–72. 10.1016/S0378-4320(99)00075-5
    1. Lessey BA, Castelbaum AJ, Sawin SW, Sun J. Integrins as markers of uterine receptivity in women with primary unexplained infertility. Fertil Steril. (1995) 63:535–42. 10.1016/S0015-0282(16)57422-6
    1. Serafim MK, Duarte AB, Silva GM, Souza CE, Magalhaes-Padilha DM, Moura AA, et al. . Impact of growth hormone (GH) and follicle stimulating hormone (FSH) on in vitro canine preantral follicle development and estradiol production. Growth Horm IGF Res. (2015) 25:85–9. 10.1016/j.ghir.2014.12.009
    1. Jeve YB, Bhandari HM. Effective treatment protocol for poor ovarian response: a systematic review and meta-analysis. J Hum Reprod Sci. (2016) 9:70–81. 10.4103/0974-1208.183515

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