The Impact of Emotional Responses on Female Reproduction: Fibrinolysis in the Spotlight

Abstract

Fibrinolytic enzymes modify various substrates required for tissue remodeling, playing a crucial role in mechanisms underlying resilience, reward processing, ovulation, embryo implantation, and placentation. Individuals with low resilience and reduced reward responsiveness, when exposed to chronic stress, are at increased risk of experiencing a range of negative emotions. Chronic anxiety and melancholia are examples of negative emotions associated with hypercortisolism, while fear and atypical depression are characterized by systemic inflammation. Both cortisol and inflammatory cytokines stimulate the production of plasminogen activator inhibitor-1 (PAI-1), a potent fibrinolysis inhibitor. Chronic anxiety, fear, and depression are among the many hypofibrinolytic conditions increasing the risk of oligo-anovulation, miscarriage, fetal growth restriction, and preeclampsia. Although significant, the impact of negative emotions on implantation is not as obvious as on ovulation or placentation. Other hypofibrinolytic conditions that may affect female reproduction through mechanisms dependent or independent of PAI-1 include metabolic disturbances (e.g., due to consumption of highly palatable foods, often used to alleviate negative affect), inflammation, hyperhomocysteinemia, hypothyroidism, hypercortisolism, antiphospholipid antibodies, and the 4G allele of the PAI-1 gene. Benzodiazepines and antidepressants should be used with caution in the first trimester as this combination may cause malformations. Also, selective serotonin reuptake inhibitors have fibrinolytic properties that increase the risk of bleeding after surgical procedures. Psychological interventions, especially group therapy, are effective in the prevention of reproductive disorders. Controlled trials are needed to test the hypothesis that female reproductive health depends on psychological well-being, a balanced diet and physical activity, suppression of inflammation and autoantibodies, and homocysteine and hormonal homeostasis.

Keywords

emotions - ovulation - embryo implantation - miscarriage - fetal growth restriction

Publikationsverlauf

Artikel online veröffentlicht:
19. Juli 2024

• References

• 1 Clifton J, Domar AD. Psychological distress and infertility: prevalence, impact, and interventions. In: Vaamonde D, Hackney AC, Garcia-Manso JM. eds. Fertility, Pregnancy, and Wellness. Amsterdam: Elsevier; 2022: 163-181
• 2 Baack ML, Wang C, Hu S, Segar JL, Norris AW. Hyperglycemia induces embryopathy, even in the absence of systemic maternal diabetes: an in vivo test of the fuel mediated teratogenesis hypothesis. Reprod Toxicol 2014; 46: 129-136
• 3 de Jersey SJ, Nicholson JM, Callaway LK, Daniels LA. A prospective study of pregnancy weight gain in Australian women. Aust N Z J Obstet Gynaecol 2012; 52 (06) 545-551
• 4 Shahsavarani A, Abadi E, Kalkhoran M. Stress: facts and theories through literature review. Intern J Med Rev 2015; 2: 230-241
• 5 McEwen BS. Central role of the brain in stress and adaptation. In: Fink G. ed. Stress: Concepts, Cognition, Emotion, and Behavior. San Diego, CA: Academic Press; 2016: 39-55
• 6 American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. DSM-5. Washington, DC: American Psychiatric Association; 2013
• 7 Martinowich K, Manji H, Lu B. New insights into BDNF function in depression and anxiety. Nat Neurosci 2007; 10 (09) 1089-1093
• 8 Irigoyen JP, Muñoz-Cánoves P, Montero L, Koziczak M, Nagamine Y. The plasminogen activator system: biology and regulation. Cell Mol Life Sci 1999; 56 (1–2): 104-132
• 9 Curry Jr TE, Smith MF. Impact of extracellular matrix remodeling on ovulation and the folliculo-luteal transition. Semin Reprod Med 2006; 24 (04) 228-241
• 10 Laurenzi G, Fedeli V, Canipari R. Decreased fertility in female mice lacking urokinase plasminogen activator. Reprod Biol 2024; 24 (01) 100840
• 11 Rizov M, Andreeva P, Dimova I. Molecular regulation and role of angiogenesis in reproduction. Taiwan J Obstet Gynecol 2017; 56 (02) 127-132
• 12 Mazur P, Sokołowski G, Hubalewska-Dydejczyk A, Płaczkiewicz-Jankowska E, Undas A. Prothrombotic alterations in plasma fibrin clot properties in thyroid disorders and their post-treatment modifications. Thromb Res 2014; 134 (02) 510-517
• 13 Hori Y, Nakatani K, Morioka K. et al. Insulin enhanced thrombin-activable fibrinolysis inhibitor expression through PI3 kinase/Akt pathway. Int J Mol Med 2005; 15 (02) 265-268
• 14 Vaughan DE. PAI-1 and atherothrombosis. J Thromb Haemost 2005; 3 (08) 1879-1883
• 15 Midorikawa S, Sanada H, Hashimoto S, Watanabe T. Enhancement by homocysteine of plasminogen activator inhibitor-1 gene expression and secretion from vascular endothelial and smooth muscle cells. Biochem Biophys Res Commun 2000; 272 (01) 182-185
• 16 Antovic A, Bruzelius M. Impaired fibrinolysis in the antiphospholipid syndrome. Semin Thromb Hemost 2021; 47 (05) 506-511
• 17 Tian R, Hou G, Li D, Yuan TF. A possible change process of inflammatory cytokines in the prolonged chronic stress and its ultimate implications for health. Sci World J 2014; 2014 (01) 780616
• 18 Parmer RJ, Mahata M, Mahata S, Sebald MT, O'Connor DT, Miles LA. Tissue plasminogen activator (t-PA) is targeted to the regulated secretory pathway. Catecholamine storage vesicles as a reservoir for the rapid release of t-PA. J Biol Chem 1997; 272 (03) 1976-1982
• 19 Moons WG, Shields GS. Anxiety, not anger, induces inflammatory activity: an avoidance/approach model of immune system activation. Emotion 2015; 15 (04) 463-476
• 20 Qiu W, Cai X, Zheng C, Qiu S, Ke H, Huang Y. Update on the relationship between depression and neuroendocrine metabolism. Front Neurosci 2021; 15: 728810
• 21 Hoirisch-Clapauch S. Mechanisms affecting brain remodeling in depression: do all roads lead to impaired fibrinolysis?. Mol Psychiatry 2022; 27 (01) 525-533
• 22 Jamar G, Ribeiro DA, Pisani LP. High-fat or high-sugar diets as trigger inflammation in the microbiota-gut-brain axis. Crit Rev Food Sci Nutr 2021; 61 (05) 836-854
• 23 Fu XY, Chen HH, Zhang N. et al. Effects of chronic unpredictable mild stress on ovarian reserve in female rats: feasibility analysis of a rat model of premature ovarian failure. Mol Med Rep 2018; 18 (01) 532-540
• 24 Zanettoullis AT, Mastorakos G, Vakas P, Vlahos N, Valsamakis G. Effect of stress on each of the stages of the IVF procedure: a systematic review. Int J Mol Sci 2024; 25 (02) 726
• 25 Klonoff-Cohen H, Chu E, Natarajan L, Sieber W. A prospective study of stress among women undergoing in vitro fertilization or gamete intrafallopian transfer. Fertil Steril 2001; 76 (04) 675-687
• 26 Dybciak P, Raczkiewicz D, Humeniuk E. et al. Depression in polycystic ovary syndrome: a systematic review and meta-analysis. J Clin Med 2023; 12 (20) 6446
• 27 Demyttenaere K, Nijs P, Evers-Kiebooms G, Koninckx PR. Coping and the ineffectiveness of coping influence the outcome of in vitro fertilization through stress responses. Psychoneuroendocrinology 1992; 17 (06) 655-665
• 28 Ny T, Wahlberg P, Brändström IJM. Matrix remodeling in the ovary: regulation and functional role of the plasminogen activator and matrix metalloproteinase systems. Mol Cell Endocrinol 2002; 187 (1–2): 29-38
• 29 Burchall GF, Piva TJ, Linden MD, Gibson-Helm ME, Ranasinha S, Teede HJ. Comprehensive assessment of the hemostatic system in polycystic ovarian syndrome. Semin Thromb Hemost 2016; 42 (01) 55-62
• 30 Petríková J, Lazúrová I. Ovarian failure and polycystic ovary syndrome. Autoimmun Rev 2012; 11 (6–7): A471-A478
• 31 Li P, Shuai P, Shen S. et al. Perturbations in gut microbiota composition in patients with polycystic ovary syndrome: a systematic review and meta-analysis. BMC Med 2023; 21 (01) 302
• 32 Machado V, Escalda C, Proença L, Mendes JJ, Botelho J. Is there a bidirectional association between polycystic ovarian syndrome and periodontitis? A systematic review and meta-analysis. J Clin Med 2020; 9 (06) 1961
• 33 Alexandraki KI, Kaltsas GA. Endocrinopathies and other disorders inducing a polycystic ovary syndrome phenotype. In: Macut D, Pfeifer M, Yildiz BO, Diamanti-Kandarakis E. eds. Polycystic Ovary Syndrome. Novel Insights into Causes and Therapy. Basel: Karger; 2013. 40. 142-157
• 34 Toulis KA, Goulis DG, Mintziori G. et al. Meta-analysis of cardiovascular disease risk markers in women with polycystic ovary syndrome. Hum Reprod Update 2011; 17 (06) 741-760
• 35 Liu Y, Sun MG, Jiang R. et al. Plasminogen activator inhibitor-1 -675 4G/5G polymorphism and polycystic ovary syndrome risk: a meta analysis. J Assist Reprod Genet 2014; 31 (03) 363-370
• 36 Cimadomo D, Rienzi L, Conforti A. et al. Opening the black box: why do euploid blastocysts fail to implant? A systematic review and meta-analysis. Hum Reprod Update 2023; 29 (05) 570-633
• 37 Gottschall JA, Gottschall TA. Are per-incident rape-pregnancy rates higher than per-incident consensual pregnancy rates?. Hum Nat 2003; 14 (01) 1-20
• 38 Wilcox AJ, Dunson DB, Weinberg CR, Trussell J, Baird DD. Likelihood of conception with a single act of intercourse: providing benchmark rates for assessment of post-coital contraceptives. Contraception 2001; 63 (04) 211-215
• 39 Kondoh E, Okamoto T, Higuchi T. et al. Stress affects uterine receptivity through an ovarian-independent pathway. Hum Reprod 2009; 24 (04) 945-953
• 40 Purewal S, Chapman SCE, van den Akker OBA. Depression and state anxiety scores during assisted reproductive treatment are associated with outcome: a meta-analysis. Reprod Biomed Online 2018; 36 (06) 646-657
• 41 Peaston G, Subramanian V, Brunckhorst O, Sarris I, Ahmed K. The impact of emotional health on assisted reproductive technology outcomes: a systematic review and meta-analysis. Hum Fertil (Camb) 2022; 25 (03) 410-421
• 42 Nicoloro-SantaBarbara J, Busso C, Moyer A, Lobel M. Just relax and you'll get pregnant? Meta-analysis examining women's emotional distress and the outcome of assisted reproductive technology. Soc Sci Med 2018; 213: 54-62
• 43 Carmeliet P, Schoonjans L, Kieckens L. et al. Physiological consequences of loss of plasminogen activator gene function in mice. Nature 1994; 368 (6470): 419-424
• 44 Axelrod HR. Altered trophoblast functions in implantation-defective mouse embryos. Dev Biol 1985; 108 (01) 185-190
• 45 Azpiroz MA, Orguilia L, Palacio MI. et al. Potential biomarkers of infertility associated with microbiome imbalances. Am J Reprod Immunol 2021; 86 (04) e13438
• 46 Pacchiarotti A, Mohamed MA, Micara G. et al. The possible role of hyperhomocysteinemia on IVF outcome. J Assist Reprod Genet 2007; 24 (10) 459-462
• 47 Zeng H, He D, Hu L, Ma W, Quan S. PAI-1 4G/4G genotype is associated with recurrent implantation failure: a systematic review and meta-analysis. Reprod Sci 2021; 28 (11) 3051-3060
• 48 Denis AL, Guido M, Adler RD, Bergh PA, Brenner C, Scott Jr RT. Antiphospholipid antibodies and pregnancy rates and outcome in in vitro fertilization patients. Fertil Steril 1997; 67 (06) 1084-1090
• 49 Jungheim ES, Schon SB, Schulte MB, DeUgarte DA, Fowler SA, Tuuli MG. IVF outcomes in obese donor oocyte recipients: a systematic review and meta-analysis. Hum Reprod 2013; 28 (10) 2720-2727
• 50 Solberg H, Rinkenberger J, Danø K, Werb Z, Lund LR. A functional overlap of plasminogen and MMPs regulates vascularization during placental development. Development 2003; 130 (18) 4439-4450
• 51 Gris JC, Ripart-Neveu S, Maugard C. et al. Prospective evaluation of the prevalence of haemostasis abnormalities in unexplained primary early recurrent miscarriages. Thromb Haemost 1997; 77 (06) 1096-1103
• 52 Qu F, Wu Y, Zhu YH. et al. The association between psychological stress and miscarriage: a systematic review and meta-analysis. Sci Rep 2017; 7 (01) 1731
• 53 Magnus MC, Havdahl A, Morken NH, Wensaas KA, Wilcox AJ, Håberg SE. Risk of miscarriage in women with psychiatric disorders. Br J Psychiatry 2021; 219 (03) 501-506
• 54 Linna MS, Raevuori A, Haukka J, Suvisaari JM, Suokas JT, Gissler M. Reproductive health outcomes in eating disorders. Int J Eat Disord 2013; 46 (08) 826-833
• 55 Almeida ND, Basso O, Abrahamowicz M, Gagnon R, Tamblyn R. Risk of miscarriage in women receiving antidepressants in early pregnancy, correcting for induced abortions. Epidemiology 2016; 27 (04) 538-546
• 56 Fabozzi G, Cimadomo D, Maggiulli R. et al. Association between oocyte donors' or recipients' body mass index and clinical outcomes after first single blastocyst transfers-the uterus is the most affected. Fertil Steril 2024; 121 (02) 281-290
• 57 Liu Y, Chen H, Feng L, Zhang J. Interactions between gut microbiota and metabolites modulate cytokine network imbalances in women with unexplained miscarriage. NPJ Biofilms Microbiomes 2021; 7 (01) 24
• 58 Choi SE, Choudhary A, Ahern JM, Palmer N, Barrow JR. Association between maternal periodontal disease and adverse pregnancy outcomes: an analysis of claims data. Fam Pract 2021; 38 (06) 718-723
• 59 Saadaoui M, Singh P, Ortashi O, Al Khodor S. Role of the vaginal microbiome in miscarriage: exploring the relationship. Front Cell Infect Microbiol 2023; 13: 1232825
• 60 Magnus MC, Morken NH, Wensaas KA, Wilcox AJ, Håberg SE. Risk of miscarriage in women with chronic diseases in Norway: a registry linkage study. PLoS Med 2021; 18 (05) e1003603
• 61 Nelen WLDM, Blom HJ, Steegers EAP, den Heijer M, Eskes TKAB. Hyperhomocysteinemia and recurrent early pregnancy loss: a meta-analysis. Fertil Steril 2000; 74 (06) 1196-1199
• 62 Zhang Y, Wang H, Pan X, Teng W, Shan Z. Patients with subclinical hypothyroidism before 20 weeks of pregnancy have a higher risk of miscarriage: a systematic review and meta-analysis. PLoS One 2017; 12 (04) e0175708
• 63 Gao R, Zeng R, Qing P. et al. Antiphospholipid antibodies and pregnancy outcome of assisted reproductive treatment: a systematic review and meta-analysis. Am J Reprod Immunol 2021; 86 (04) e13470
• 64 Wen Y, He H, Zhao K. Thrombophilic gene polymorphisms and recurrent pregnancy loss: a systematic review and meta-analysis. J Assist Reprod Genet 2023; 40 (07) 1533-1558
• 65 Iliodromiti S, Mackay DF, Smith GCS. et al. Customised and noncustomised birth weight centiles and prediction of stillbirth and infant mortality and morbidity: a cohort study of 979,912 term singleton pregnancies in Scotland. PLoS Med 2017; 14 (01) e1002228
• 66 Bussières EL, Tarabulsy GM, Pearson J, Tessier R, Forest JC, Giguère Y. Maternal prenatal stress and infant birth weight and gestational age: a meta-analysis of prospective studies. Dev Rev 2015; 36: 179-199
• 67 Al-Azemi M, Raghupathy R, Azizieh F. Pro-inflammatory and anti-inflammatory cytokine profiles in fetal growth restriction. Clin Exp Obstet Gynecol 2017; 44 (01) 98-103
• 68 Kırıcı P, Çağıran FT, Kalı Z, Tanrıverdi ES, Mavral N, Ecin SM. Determination of maternal serum pro-inflammatory cytokine changes in intrauterine growth restriction. Eur Rev Med Pharmacol Sci 2023; 27 (05) 1996-2001
• 69 Ghimire U, Papabathini SS, Kawuki J, Obore N, Musa TH. Depression during pregnancy and the risk of low birth weight, preterm birth and intrauterine growth restriction- an updated meta-analysis. Early Hum Dev 2021; 152: 105243
• 70 Yang Z, Wang X, Wang M, Yan S, Wu F, Zhang F. Trajectory of prenatal anxiety and depression and its association with fetal growth development. Early Hum Dev 2023; 187: 105875
• 71 Shriyan P, Sudhir P, van Schayck OCP, Babu GR. Association of high cortisol levels in pregnancy and altered fetal growth. Results from the MAASTHI, a prospective cohort study, Bengaluru. Lancet Reg Health Southeast Asia 2023; 14: 100196
• 72 Reynolds LP, Vonnahme KA, Lemley CO. et al. Maternal stress and placental vascular function and remodeling. Curr Vasc Pharmacol 2013; 11 (05) 564-593
• 73 Castrogiovanni D, Alzamendi A, Ongaro L, Giovambattista A, Gaillard RC, Spinedi E. Fructose rich diet-induced high plasminogen activator inhibitor-1 (PAI-1) production in the adult female rat: protective effect of progesterone. Nutrients 2012; 4 (08) 1137-1150
• 74 Piccinni MP, Raghupathy R, Saito S, Szekeres-Bartho J. Cytokines, hormones and cellular regulatory mechanisms favoring successful reproduction. Front Immunol 2021; 12: 717808
• 75 Tanner LD, Brock And C, Chauhan SP. Severity of fetal growth restriction stratified according to maternal obesity. J Matern Fetal Neonatal Med 2022; 35 (10) 1886-1890
• 76 Carvalheiras G, Faria R, Braga J, Vasconcelos C. Fetal outcome in autoimmune diseases. Autoimmun Rev 2012; 11 (6–7): A520-A530
• 77 Hoirisch-Clapauch S. Silicone breast implants may contribute to early-onset fetal growth restriction. Clin Rheumatol 2023; 42 (09) 2445-2452
• 78 Tao Z, Chen Y, He F. et al. Alterations in the gut microbiome and metabolisms in pregnancies with fetal growth restriction. Microbiol Spectr 2023; 11 (03) e0007623
• 79 Ziaei S, Norrozi M, Faghihzadeh S, Jafarbegloo E. A randomised placebo-controlled trial to determine the effect of iron supplementation on pregnancy outcome in pregnant women with haemoglobin > or = 13.2 g/dl. BJOG 2007; 114 (06) 684-688
• 80 Díaz-Torres S, Díaz-López A, Arija V. Effect of prenatal iron supplementation adapted to hemoglobin levels in early pregnancy on fetal and neonatal growth—ECLIPSES Study. Nutrients 2024; 16 (03) 437
• 81 Xu J, Zhou F, Wang X, Mo C. Role of ferroptosis in pregnancy related diseases and its therapeutic potential. Front Cell Dev Biol 2023; 11: 1083838
• 82 Hogeveen M, Blom HJ, den Heijer M. Maternal homocysteine and small-for-gestational-age offspring: systematic review and meta-analysis. Am J Clin Nutr 2012; 95 (01) 130-136
• 83 Silva JF, Vidigal PN, Galvão DD. et al. Fetal growth restriction in hypothyroidism is associated with changes in proliferative activity, apoptosis and vascularisation of the placenta. Reprod Fertil Dev 2012; 24 (07) 923-931
• 84 Lindsay JR, Jonklaas J, Oldfield EH, Nieman LK. Cushing's syndrome during pregnancy: personal experience and review of the literature. J Clin Endocrinol Metab 2005; 90 (05) 3077-3083
• 85 Xu J, Chen D, Tian Y, Wang X, Peng B. Antiphospholipid antibodies increase the risk of fetal growth restriction: a systematic meta-analysis. Int J Clin Pract 2022; 2022: 4308470
• 86 Infante-Rivard C, Rivard GE, Guiguet M, Gauthier R. Thrombophilic polymorphisms and intrauterine growth restriction. Epidemiology 2005; 16 (03) 281-287
• 87 Said JM, Tsui R, Borg AJ. et al. The PAI-1 4G/5G polymorphism is not associated with an increased risk of adverse pregnancy outcome in asymptomatic nulliparous women. J Thromb Haemost 2012; 10 (05) 881-886
• 88 Ye Y, Vattai A, Zhang X. et al. Role of plasminogen activator inhibitor type 1 in pathologies of female reproductive diseases. Int J Mol Sci 2017; 18 (08) 1651
• 89 Greenberg KI, Choi MJ. Understanding hypercoagulability with nephrotic syndrome: how the clot thickens. Clin J Am Soc Nephrol 2023; 18 (02) 149-151
• 90 Malyszko J, Skrzydlewska E, Malyszko JS, Myśliwiec M. Protein Z, a vitamin K-dependent protein in patients with renal failure. J Thromb Haemost 2003; 1 (01) 195-196
• 91 Ogawa M, Matsuda Y, Kobayashi A, Mitani M, Makino Y, Matsui H. Plasma antithrombin levels correlate with albumin and total protein in gestational hypertension and preeclampsia. Pregnancy Hypertens 2014; 4 (02) 174-177
• 92 Weenink GH, Treffers PE, Vijn P, Smorenberg-Schoorl ME, Ten Cate JW. Antithrombin III levels in preeclampsia correlate with maternal and fetal morbidity. Am J Obstet Gynecol 1984; 148 (08) 1092-1097
• 93 Erez O, Hoppensteadt D, Romero R. et al. Preeclampsia is associated with low concentrations of protein Z. J Matern Fetal Neonatal Med 2007; 20 (09) 661-667
• 94 Nielsen LH, Kronborg C, Vittinghus E. et al. Is urinary excretion of plasminogen associated with development of pre-eclampsia? An observational, explorative case-control study. BMJ Open 2019; 9 (06) e026489
• 95 Baran Ö, Tuncer M, Nergiz Y, Akkuş M, Erdemoğlu M, Büyükbayram H. An increase of elastic tissue fibers in blood vessel walls of placental stem villi and differences in the thickness of blood vessel walls in third trimester pre-eclampsia pregnancies. Open Med 2010; 5 (02) 227-234
• 96 Agersnap I, Nissen PH, Hvas AM. The role of plasminogen activator inhibitor type 1 (PAI-1) in placenta-mediated pregnancy complications: a systematic review. Semin Thromb Hemost 2022; 48 (05) 607-624
• 97 Bodova KB, Biringer K, Dokus K, Ivankova J, Stasko J, Danko J. Fibronectin, plasminogen activator inhibitor type 1 (PAI-1) and uterine artery Doppler velocimetry as markers of preeclampsia. Dis Markers 2011; 30 (04) 191-196
• 98 Qiu C, Williams MA, Calderon-Margalit R, Cripe SM, Sorensen TK. Preeclampsia risk in relation to maternal mood and anxiety disorders diagnosed before or during early pregnancy. Am J Hypertens 2009; 22 (04) 397-402
• 99 Almasi-Hashiani A, Omani-Samani R, Mohammadi M. et al. Assisted reproductive technology and the risk of preeclampsia: an updated systematic review and meta-analysis. BMC Pregnancy Childbirth 2019; 19 (01) 149
• 100 Paula WO, Patriota ESO, Gonçalves VSS, Pizato N. Maternal consumption of ultra-processed foods-rich diet and perinatal outcomes: a systematic review and meta-analysis. Nutrients 2022; 14 (15) 3242
• 101 Gallos ID, Sivakumar K, Kilby MD, Coomarasamy A, Thangaratinam S, Vatish M. Pre-eclampsia is associated with, and preceded by, hypertriglyceridaemia: a meta-analysis. BJOG 2013; 120 (11) 1321-1332
• 102 Xiong Z, Wang Q, Pei S, Zhu Z. The causal role of intestinal microbiome in development of pre-eclampsia. Funct Integr Genomics 2023; 23 (02) 127
• 103 He XJ, Dai RX, Hu CL. Maternal prepregnancy overweight and obesity and the risk of preeclampsia: a meta-analysis of cohort studies. Obes Res Clin Pract 2020; 14 (01) 27-33
• 104 Hu H, Ha S, Roth J, Kearney G, Talbott EO, Xu X. Ambient air pollution and hypertensive disorders of pregnancy: a systematic review and meta-analysis. Atmos Environ 2014; 97: 336-345
• 105 Dong Y, Yuan F, Dai Z, Wang Z, Zhu Y, Wang B. Preeclampsia in systemic lupus erythematosus pregnancy: a systematic review and meta-analysis. Clin Rheumatol 2020; 39 (02) 319-325
• 106 Köcher L, Rossides M, Remaeus K. et al. Maternal and infant outcomes in sarcoidosis pregnancy: a Swedish population-based cohort study of first births. Respir Res 2020; 21 (01) 225
• 107 Conde-Agudelo A, Romero R. SARS-CoV-2 infection during pregnancy and risk of preeclampsia: a systematic review and meta-analysis. Am J Obstet Gynecol 2022; 226 (01) 68-89.e3
• 108 Nourollahpour Shiadeh M, Behboodi Moghadam Z, Adam I, Saber V, Bagheri M, Rostami A. Human infectious diseases and risk of preeclampsia: an updated review of the literature. Infection 2017; 45 (05) 589-600
• 109 Shan Y, Guan C, Wang J, Qi W, Chen A, Liu S. Impact of ferroptosis on preeclampsia: a review. Biomed Pharmacother 2023; 167: 115466
• 110 Zhang C, Hu J, Wang X, Gu H. High level of homocysteine is associated with pre-eclampsia risk in pregnant woman: a meta-analysis. Gynecol Endocrinol 2022; 38 (09) 705-712
• 111 Hajifoghaha M, Teshnizi SH, Forouhari S, Dabbaghmanesh MH. Association of thyroid function test abnormalities with preeclampsia: a systematic review and meta-analysis. BMC Endocr Disord 2022; 22 (01) 240
• 112 Caimari F, Valassi E, Garbayo P. et al. Cushing's syndrome and pregnancy outcomes: a systematic review of published cases. Endocrine 2017; 55 (02) 555-563
• 113 Walter IJ, Klein Haneveld MJ, Lely AT, Bloemenkamp KWM, Limper M, Kooiman J. Pregnancy outcome predictors in antiphospholipid syndrome: a systematic review and meta-analysis. Autoimmun Rev 2021; 20 (10) 102901
• 114 Zhao L, Bracken MB, Dewan AT, Chen S. Association between the SERPINE1 (PAI-1) 4G/5G insertion/deletion promoter polymorphism (rs1799889) and pre-eclampsia: a systematic review and meta-analysis. Mol Hum Reprod 2013; 19 (03) 136-143
• 115 Wang X, Khalil RA. Matrix metalloproteinases, vascular remodeling, and vascular disease. In: Raouf A. Khalil, ed. Advances in Pharmacology. Vol. 18. Cambridge, MA: Academic Press; 2018: 241-330
• 116 Atiomo WU, Bates SA, Condon JE, Shaw S, West JH, Prentice AG. The plasminogen activator system in women with polycystic ovary syndrome. Fertil Steril 1998; 69 (02) 236-241
• 117 Targher G, Zoppini G, Bonora E, Moghetti P. Hemostatic and fibrinolytic abnormalities in polycystic ovary syndrome. Semin Thromb Hemost 2014; 40 (05) 600-618
• 118 Martínez-Zamora MA, Creus M, Tassies D. et al. Reduced plasma fibrinolytic potential in patients with recurrent implantation failure after IVF and embryo transfer. Hum Reprod 2011; 26 (03) 510-516
• 119 Rai R, Tuddenham E, Backos M. et al. Thromboelastography, whole-blood haemostasis and recurrent miscarriage. Hum Reprod 2003; 18 (12) 2540-2543
• 120 Marchi R, López Ramirez Y, Nagaswami C. et al. Haemostatic changes related to fibrin formation and fibrinolysis during the first trimester in normal pregnancy and in recurrent miscarriage. Thromb Haemost 2007; 97 (04) 552-557
• 121 Wang M, Hu Z, Cheng QX, Xu J, Liang C. The ability of thromboelastography parameters to predict severe pre-eclampsia when measured during early pregnancy. Int J Gynaecol Obstet 2019; 145 (02) 170-175
• 122 Ohnishi J, Ohnishi E, Shibuya H, Takahashi T. Functions for proteinases in the ovulatory process. Biochim Biophys Acta 2005; 1751 (01) 95-109
• 123 Qu H, Khalil RA. Role of ADAM and ADAMTS disintegrin and metalloproteinases in normal pregnancy and preeclampsia. Biochem Pharmacol 2022; 206: 115266
• 124 El-Osta A, Brasacchio D, Yao D. et al. Transient high glucose causes persistent epigenetic changes and altered gene expression during subsequent normoglycemia. J Exp Med 2008; 205 (10) 2409-2417
• 125 Rajaram S, Gupta V, Gupta B. Unexplained recurrent miscarriage: a dilemma. In: Mehta S, Gupta B. Eds. Recurrent Pregnancy Loss. Singapore: Springer; 2018: 149-156
• 126 Bian C, Cao J, Chen K, Xia X, Yu X. Effectiveness of psychological interventions on pregnancy rates in infertile women undergoing assisted reproductive technologies: a meta-analysis of randomised controlled trials. Biotechnol Genet Eng Rev 2023; 1-20
• 127 Warne E, Oxlad M, Best T. Evaluating group psychological interventions for mental health in women with infertility undertaking fertility treatment: a systematic review and meta-analysis. Health Psychol Rev 2023; 17 (03) 377-401
• 128 Grigoriadis S, Graves L, Peer M. et al. Benzodiazepine use during pregnancy alone or in combination with an antidepressant and congenital malformations: systematic review and meta-analysis. J Clin Psychiatry 2019; 80 (04) 1845
• 129 Teede HJ, Misso ML, Costello MF. et al; International PCOS Network. Recommendations from the international evidence-based guideline for the assessment and management of polycystic ovary syndrome. Clin Endocrinol (Oxf) 2018; 89 (03) 251-268
• 130 Doutremepuich C, Deharo E, Doutremepuich F, Lalanne MC, Toulemonde F. Kinetic study of tPA release induced by heparin and heparin fragment. Thromb Res 1989; 53 (06) 615-621
• 131 Tiscia GL, De Laurenzo A, Cappucci F. et al. Thromboelastography parameters in Italian pregnant women: do antithrombotic drugs change reference values?. J Investig Med 2020; 68 (04) 902-905
• 132 Hoirisch-Clapauch S, Nardi AE. Autism spectrum disorders: let's talk about glucose?. Transl Psychiatry 2019; 9 (01) 51
• 133 Yan YS, Feng C, Yu DQ. et al. Long-term outcomes and potential mechanisms of offspring exposed to intrauterine hyperglycemia. Front Nutr 2023; 10: 1067282
• 134 Hu Z, Gao R, Huang W, Wang H, Qin L. Effect of hydroxychloroquine on lupus activity, preeclampsia and intrauterine growth restriction in pregnant women with systemic lupus erythematosus and/or antiphospholipid syndrome: a systematic review and meta-analysis. J Clin Med 2023; 12 (02) 485