Oxidative stress in pregnancy and fertility pathologies

Cell Biology and Toxicology

Volumn 30, Issue 5, 2014, Pages 301-312

  Pereira, Ana C ^a,b   Martel, Fátima ^b  

^a POLYTECHNIC INSTITUTE OF PORTO   (Portugal)

^b University of Porto   (Portugal)

Author keywords

Oxidative stress; Placenta; Pregnancy disorders; Reactive oxygen species

Indexed keywords

ANTIOXIDANT; REACTIVE OXYGEN METABOLITE;

FEMALE; FERTILITY; HUMAN; METABOLISM; OXIDATIVE STRESS; PATHOLOGY; PHYSIOLOGY; PLACENTA; PREGNANCY;

ANTIOXIDANTS; FEMALE; FERTILITY; HUMANS; OXIDATIVE STRESS; PLACENTA; PREGNANCY; REACTIVE OXYGEN SPECIES;

EID: 84930797728     PISSN: 07422091     EISSN: 15736822     Source Type: Journal    
DOI: 10.1007/s10565-014-9285-2     Document Type: Review

References (98)

1. Agarwal A, Gupta S, Sharma RK. Role of oxidative stress in female reproduction. Reprod Biol Endocrinol. 2005;3:28.
2. Agarwal A, Aponte-Mellado A, Premkumar BJ, Shaman A, Gupta S. The effects of oxidative stress on female reproduction: a review. Reprod Biol Endocrinol. 2012;10:49.
3. Aherne SA, O'Brien NM. Mechanism of protection by the flavonoids, quercetin and rutin, against tert-butylhydroperoxide- and menadione-induced DNA single strand breaks in Caco-2 cells. Free Radic Biol Med. 2000;29:507–14.
4. Al-Shebly MM, Mansour MA. Evaluation of oxidative stress and antioxidant status in diabetic and hypertensive women during labor. Oxid Med Cell Longev. 2012;2012:329743.
5. Andrade, A.Z., J.K. Rodrigues, L.A. Dib, G.S. Romão, R.A. Ferriani, A.A. Jordão Junior, and P.A. Navarro. Serum markers of oxidative stress in infertile women with endometriosis. Rev Bras Ginecol Obstet. 2010;32:279–285.
6. Araújo JR, Ramalho C, Correia-Branco A, Faria A, Ferraz T, Keating E, et al. A parallel increase in placental oxidative stress and antioxidant defenses occurs in pre-gestational type 1 but not gestational diabetes. Placenta. 2013;34:1095–8.
7. Asemi Z, Samimi M, Tabassi Z, Sabihi SS, Esmaillzadeh A. A randomized controlled clinical trial investigating the effect of DASH diet on insulin resistance, inflammation, and oxidative stress in gestational diabetes. Nutrition. 2013;29:619–24.
8. Augoulea A, Mastorakos G, Lambrinoudaki I, Christodoulakos G, Creatsas G. The role of the oxidative-stress in the endometriosis-related infertility. Gynecol Endocrinol. 2009;25:75–81.
9. Badawy A, State O, Abdelgawad S. N-acetyl cysteine and clomiphene citrate for induction of ovulation in polycystic ovary syndrome: a cross-over trial. Acta Obstet Gynecol Scand. 2007;86:218–22.
10. Badr G, Alwasel S, Ebaid H, Mohany M, Alhazza I. Perinatal supplementation with thymoquinone improves diabetic complications and T cell immune responses in rat offspring. Cell Immunol. 2011;267:133–40.
11. Biri A, Bozkurt N, Turp A, Kavutcu M, Himmetoglu O, Durak I. Role of oxidative stress in intrauterine growth restriction. Gynecol Obstet Invest. 2007;64:187–92.
12. Blair SA, Kyaw-Tun T, Young IS, Phelan NA, Gibney J, McEneny J. Oxidative stress and inflammation in lean and obese subjects with polycystic ovary syndrome. J Reprod Med. 2013;58:107–14.
13. Boomsma CM, Eijkemans MJ, Hughes EG, Visser GH, Fauser BC, Macklon NS. A meta-analysis of pregnancy outcomes in women with polycystic ovary syndrome. Hum Reprod Update. 2006;12:673–83.
14. Boutzios G, Livadas S, Piperi C, Vitoratos N, Adamopoulos C, Hassiakos D, et al. Polycystic ovary syndrome offspring display increased oxidative stress markers comparable to gestational diabetes offspring. Fertil Steril. 2013;99:943–50.
15. Burton GJ, Jauniaux E. Oxidative stress. Best Pract Res Clin Obstet Gynaecol. 2011;25:287–99.
16. Burton, G.J., H.W. Yung, T. Cindrova-Davies, and D.S. Charnock-Jones. Placental endoplasmic reticulum stress and oxidative stress in the pathophysiology of unexplained intrauterine growth restriction and early onset preeclampsia. Placenta. 2009;30 Suppl A:S43-48.
17. Burton GJ, Jauniaux E, Charnock-Jones DS. The influence of the intrauterine environment on human placental development. Int J Dev Biol. 2010;54:303–12.
18. Campos Petean C, Ferriani RA, dos Reis RM, de Moura MD, Jordão AA, Navarro PA. Lipid peroxidation and vitamin E in serum and follicular fluid of infertile women with peritoneal endometriosis submitted to controlled ovarian hyperstimulation: a pilot study. Fertil Steril. 2008;90:2080–5.
19. Carvalho LF, Abrão MS, Biscotti C, Sharma R, Nutter B, Falcone T. Oxidative cell injury as a predictor of endometriosis progression. Reprod Sci. 2013;20:688–98.
20. Cederberg J, Simán CM, Eriksson UJ. Combined treatment with vitamin E and vitamin C decreases oxidative stress and improves fetal outcome in experimental diabetic pregnancy. Pediatr Res. 2001;49:755–62.
21. Coughlan MT, Permezel M, Georgiou HM, Rice GE. Repression of oxidant-induced nuclear factor-kappaB activity mediates placental cytokine responses in gestational diabetes. J Clin Endocrinol Metab. 2004a;89:3585–94.
22. Coughlan MT, Vervaart PP, Permezel M, Georgiou HM, Rice GE. Altered placental oxidative stress status in gestational diabetes mellitus. Placenta. 2004b;25:78–84.
23. Dalle-Donne I, Rossi R, Giustarini D, Milzani A, Colombo R. Protein carbonyl groups as biomarkers of oxidative stress. Clin Chim Acta. 2003;329:23–38.
24. Dalle-Donne I, Rossi R, Colombo R, Giustarini D, Milzani A. Biomarkers of oxidative damage in human disease. Clin Chem. 2006;52:601–23.
25. Dröge W. Free radicals in the physiological control of cell function. Physiol Rev. 2002;82:47–95.
26. Eriksson UJ, Simán CM. Pregnant diabetic rats fed the antioxidant butylated hydroxytoluene show decreased occurrence of malformations in offspring. Diabetes. 1996;45:1497–502.
27. Fujimaki A, Watanabe K, Mori T, Kimura C, Shinohara K, Wakatsuki A. Placental oxidative DNA damage and its repair in preeclamptic women with fetal growth restriction. Placenta. 2011;32:367–72.
28. Garite TJ, Clark R, Thorp JA. Intrauterine growth restriction increases morbidity and mortality among premature neonates. Am J Obstet Gynecol. 2004;191:481–7.
29. Gauster M, Desoye G, Tötsch M, Hiden U. The placenta and gestational diabetes mellitus. Curr Diab Rep. 2012;12:16–23.
30. Giudice LC, Kao LC. Endometriosis. Lancet. 2004;364:1789–99.
31. Gupta S, Agarwal A, Krajcir N, Alvarez JG. Role of oxidative stress in endometriosis. Reprod Biomed Online. 2006;13:126–34.
32. Halliwell B. Oxidative stress in cell culture: an under-appreciated problem? FEBS Lett. 2003;540:3–6.
33. Hempstock J, Jauniaux E, Greenwold N, Burton GJ. The contribution of placental oxidative stress to early pregnancy failure. Hum Pathol. 2003;34:1265–75.
34. Hracsko Z, Orvos H, Novak Z, Pal A, Varga IS. Evaluation of oxidative stress markers in neonates with intra-uterine growth retardation. Redox Rep. 2008;13:11–6.
35. Jackson LW, Schisterman EF, Dey-Rao R, Browne R, Armstrong D. Oxidative stress and endometriosis. Hum Reprod. 2005;20:2014–20.
36. Jauniaux E, Gulbis B, Burton GJ. Physiological implications of the materno-fetal oxygen gradient in human early pregnancy. Reprod Biomed Online. 2003;7:250–3.
37. Kamath U, Rao G, Kamath SU, Rai L. Maternal and fetal indicators of oxidative stress during intrauterine growth retardation (IUGR). Indian J Clin Biochem. 2006;21:111–5.
38. Karowicz-Bilińska A, Suzin J, Sieroszewski P. Evaluation of oxidative stress indices during treatment in pregnant women with intrauterine growth retardation. Med Sci Monit. 2002;8:211–6.
39. Kurdoglu Z, Ozkol H, Tuluce Y, Koyuncu I. Oxidative status and its relation with insulin resistance in young non-obese women with polycystic ovary syndrome. J Endocrinol Invest. 2012;35:317–21.
40. Lambrinoudaki IV, Augoulea A, Christodoulakos GE, Economou EV, Kaparos G, Kontoravdis A, et al. Measurable serum markers of oxidative stress response in women with endometriosis. Fertil Steril. 2009;91:46–50.
41. Lappas M, Mitton A, Mittion A, Permezel M. In response to oxidative stress, the expression of inflammatory cytokines and antioxidant enzymes are impaired in placenta, but not adipose tissue, of women with gestational diabetes. J Endocrinol. 2010;204:75–84.
42. Leach L, Taylor A, Sciota F. Vascular dysfunction in the diabetic placenta: causes and consequences. J Anat. 2009;215:69–76.
43. Ley SH, Hanley AJ, Sermer M, Zinman B, O'Connor DL. Lower dietary vitamin E intake during the second trimester is associated with insulin resistance and hyperglycemia later in pregnancy. Eur J Clin Nutr. 2013;67:1154–6.
44. Liang HY, Hou F, Ding YL, Zhang WN, Huang XH, Zhang BY, et al. Clinical evaluation of the antioxidant activity of astragalus in women with gestational diabetes. Nan Fang Yi Ke Da Xue Xue Bao. 2009;29:1402–4.
45. Liu J, Zhang D. The role of oxidative stress in the pathogenesis of polycystic ovary syndrome. Sichuan Da Xue Xue Bao Yi Xue Ban. 2012;43:187–90.
46. Lorenzoni F, Giampietri M, Ferri G, Lunardi S, Madrigali V, Battini L, et al. Lutein administration to pregnant women with gestational diabetes mellitus is associated to a decrease of oxidative stress in newborns. Gynecol Endocrinol. 2013;29:901–3.
47. Macut D, Simic T, Lissounov A, Pljesa-Ercegovac M, Bozic I, Djukic T, et al. Insulin resistance in non-obese women with polycystic ovary syndrome: relation to byproducts of oxidative stress. Exp Clin Endocrinol Diabetes. 2011;119:451–5.
48. Makni M, Sefi M, Garoui EM, Fetoui H, Boudawara T, Zeghal N. Dietary polyunsaturated fatty acid prevents hyperlipidemia and hepatic oxidant status in pregnant diabetic rats and their macrosomic offspring. J Diabetes Complications. 2011;25:267–74.
49. Mandruzzato G, Antsaklis A, Botet F, Chervenak FA, Figueras F, Grunebaum A, et al. Intrauterine restriction (IUGR). J Perinat Med. 2008;36:277–81.
50. Masharani U, Gjerde C, Evans JL, Youngren JF, Goldfine ID. Effects of controlled-release alpha lipoic acid in lean, nondiabetic patients with polycystic ovary syndrome. J Diabetes Sci Technol. 2010;4:359–64.
51. Matsuzaki S, Schubert B. Oxidative stress status in normal ovarian cortex surrounding ovarian endometriosis. Fertil Steril. 2010;93:2431–2.
52. Mert I, Oruc AS, Yuksel S, Cakar ES, Buyukkagnici U, Karaer A, et al. Role of oxidative stress in preeclampsia and intrauterine growth restriction. J Obstet Gynaecol Res. 2012;38:658–64.
53. Mier-Cabrera J, Aburto-Soto T, Burrola-Méndez S, Jiménez-Zamudio L, Tolentino MC, Casanueva E, et al. Women with endometriosis improved their peripheral antioxidant markers after the application of a high antioxidant diet. Reprod Biol Endocrinol. 2009;7:54.
54. Mier-Cabrera J, Jiménez-Zamudio L, García-Latorre E, Cruz-Orozco O, Hernández-Guerrero C. Quantitative and qualitative peritoneal immune profiles, T-cell apoptosis and oxidative stress-associated characteristics in women with minimal and mild endometriosis. BJOG. 2011;118:6–16.
55. Mitjavila MT, Moreno JJ. The effects of polyphenols on oxidative stress and the arachidonic acid cascade. Implications for the prevention/treatment of high prevalence diseases. Biochem Pharmacol. 2012;84:1113–22.
56. Montuschi P, Barnes PJ, Roberts LJ. Isoprostanes: markers and mediators of oxidative stress. FASEB J. 2004;18:1791–800.
57. Morrow JD, Awad JA, Boss HJ, Blair IA, Roberts LJ. Non-cyclooxygenase-derived prostanoids (F2-isoprostanes) are formed in situ on phospholipids. Proc Natl Acad Sci U S A. 1992;89:10721–5.
58. Myatt L. Review: reactive oxygen and nitrogen species and functional adaptation of the placenta. Placenta. 2010;31(Suppl):S66–9.
59. Myatt L, Cui X. Oxidative stress in the placenta. Histochem Cell Biol. 2004;122:369–82.
60. Nasr A. Effect of N-acetyl-cysteine after ovarian drilling in clomiphene citrate-resistant PCOS women: a pilot study. Reprod Biomed Online. 2010;20:403–9.
61. Polak G, Kotarski J. Total oxidative status of peritoneal fluid in women with endometriosis. Ginekol Pol. 2010;81:922–5.
62. Polak G, Rola R, Gogacz M, Kozioł-Montewka M, Kotarski J. Malonyldialdehyde and total antioxidant status in the peritoneal fluid of infertile women. Ginekol Pol. 1999;70:135–40.
63. Polak G, Kozioł-Montewka M, Gogacz M, Błaszkowska I, Kotarski J. Total antioxidant status of peritoneal fluid in infertile women. Eur J Obstet Gynecol Reprod Biol. 2001a;94:261–3.
64. Polak G, Kozioł-Montewka M, Tarkowski R, Kotarski J. Peritoneal fluid and plasma 4-hydroxynonenal and malonyldialdehyde concentrations in infertile women. Ginekol Pol. 2001b;72:1316–20.
65. Poli G, Leonarduzzi G, Biasi F, Chiarpotto E. Oxidative stress and cell signalling. Curr Med Chem. 2004;11:1163–82.
66. Poston L, Raijmakers MT. Trophoblast oxidative stress, antioxidants and pregnancy outcome—a review. Placenta. 2004;25(A):S72–8.
67. Poston L, Igosheva N, Mistry HD, Seed PT, Shennan AH, Rana S, et al. Role of oxidative stress and antioxidant supplementation in pregnancy disorders. Am J Clin Nutr. 2011;94:1980S–5S.
68. Radomski D, Orzechowska A, Barcz E. Present conceptions of etiopathogenesis of polycystic ovary syndrome. Ginekol Pol. 2007;78:393–9.
69. Raijmakers MT, Dechend R, Poston L. Oxidative stress and preeclampsia: rationale for antioxidant clinical trials. Hypertension. 2004;44:374–80.
70. Rizk AY, Bedaiwy MA, Al-Inany HG. N-acetyl-cysteine is a novel adjuvant to clomiphene citrate in clomiphene citrate-resistant patients with polycystic ovary syndrome. Fertil Steril. 2005;83:367–70.
71. Roberts JM, August PA, Bakris G, Barton JR, Bernstein IM, Druzin M, et al. Hypertension in pregnancy. Report American College Obstetricians Gynecologists’ Task Force Hypertension Pregnancy. Obstet Gynecol. 2013;122(5):1122–31.
72. Rong R, Ramachandran S, Santanam N, Murphy AA, Parthasarathy S. Induction of monocyte chemotactic protein-1 in peritoneal mesothelial and endometrial cells by oxidized low-density lipoprotein and peritoneal fluid from women with endometriosis. Fertil Steril. 2002;78:843–8.
73. Roos N, Kieler H, Sahlin L, Ekman-Ordeberg G, Falconer H, Stephansson O. Risk of adverse pregnancy outcomes in women with polycystic ovary syndrome: population based cohort study. BMJ. 2011;343:d6309.
74. Ruder EH, Hartman TJ, Blumberg J, Goldman MB. Oxidative stress and antioxidants: exposure and impact on female fertility. Hum Reprod Update. 2008;14:345–57.
75. Rumbold, A., P. Middleton, and C.A. Crowther. Vitamin supplementation for preventing miscarriage. Cochrane Database Syst Rev. 2005;CD004073.
76. Sacks DA, Hadden DR, Maresh M, Deerochanawong C, Dyer AR, Metzger BE, et al. Frequency of gestational diabetes mellitus at collaborating centers based on IADPSG consensus panel-recommended criteria: the Hyperglycemia and Adverse Pregnancy Outcome (HAPO) Study. Diabetes Care. 2012;35:526–8.
77. Sakamaki H, Akazawa S, Ishibashi M, Izumino K, Takino H, Yamasaki H, et al. Significance of glutathione-dependent antioxidant system in diabetes-induced embryonic malformations. Diabetes. 1999;48:1138–44.
78. Salehpour S, Sene AA, Saharkhiz N, Sohrabi MR, Moghimian F. N-acetylcysteine as an adjuvant to clomiphene citrate for successful induction of ovulation in infertile patients with polycystic ovary syndrome. J Obstet Gynaecol Res. 2012;38:1182–6.
79. Salmon AB, Richardson A, Pérez VI. Update on the oxidative stress theory of aging: does oxidative stress play a role in aging or healthy aging? Free Radic Biol Med. 2010;48:642–55.
80. Santanam N, Kavtaradze N, Murphy A, Dominguez C, Parthasarathy S. Antioxidant supplementation reduces endometriosis-related pelvic pain in humans. Transl Res. 2013;161:189–95.
81. Scifres CM, Nelson DM. Intrauterine growth restriction, human placental development and trophoblast cell death. J Physiol. 2009;587:3453–8.
82. Sharma I, Dhaliwal LK, Saha SC, Sangwan S, Dhawan V. Role of 8-iso-prostaglandin F2alpha and 25-hydroxycholesterol in the pathophysiology of endometriosis. Fertil Steril. 2010;94:63–70.
83. Shibata M, Hakuno F, Yamanaka D, Okajima H, Fukushima T, Hasegawa T, et al. Paraquat-induced oxidative stress represses phosphatidylinositol 3-kinase activities leading to impaired glucose uptake in 3T3-L1 adipocytes. J Biol Chem. 2010;285:20915–25.
84. SHUTE EV. Should spontaneous abortion be prevented? Vitamin E in its management. Can Med Assoc J. 1960;82:72–6.
85. Silva E, Soares-da-Silva P. Reactive oxygen species and the regulation of renal Na+-K+-ATPase in opossum kidney cells. Am J Physiol Regul Integr Comp Physiol. 2007;293:R1764–70.
86. Simán CM, Eriksson UJ. Vitamin C supplementation of the maternal diet reduces the rate of malformation in the offspring of diabetic rats. Diabetologia. 1997a;40:1416–24.
87. Simán CM, Eriksson UJ. Vitamin E decreases the occurrence of malformations in the offspring of diabetic rats. Diabetes. 1997b;46:1054–61.
88. Sugimura Y, Murase T, Kobayashi K, Oyama K, Hayasaka S, Kanou Y, et al. Alpha-lipoic acid reduces congenital malformations in the offspring of diabetic mice. Diabetes Metab Res Rev. 2009;25:287–94.
89. Takagi Y, Nikaido T, Toki T, Kita N, Kanai M, Ashida T, et al. Levels of oxidative stress and redox-related molecules in the placenta in preeclampsia and fetal growth restriction. Virchows Arch. 2004;444:49–55.
90. Tarín JJ, Pérez-Albalá S, Cano A. Consequences on offspring of abnormal function in ageing gametes. Hum Reprod Update. 2000;6:532–49.
91. Theuerkauf RS, Ahammer H, Siwetz M, Helige C, Dohr G, Walcher W, et al. Measurement of cell death by oxidative stress in three-dimensional spheroids from trophoblast and in fragments of decidua tissue. J Reprod Immunol. 2010;85:63–70.
92. Tuuli MG, Longtine MS, Nelson DM. Review: oxygen and trophoblast biology—a source of controversy. Placenta. 2011;32 Suppl 2:S109–18.
93. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol. 2007;39:44–84.
94. Victor VM, Rocha M, Bañuls C, Alvarez A, de Pablo C, Sanchez-Serrano M, et al. Induction of oxidative stress and human leukocyte/endothelial cell interactions in polycystic ovary syndrome patients with insulin resistance. J Clin Endocrinol Metab. 2011;96:3115–22.
95. Wang Y, Sharma RK, Falcone T, Goldberg J, Agarwal A. Importance of reactive oxygen species in the peritoneal fluid of women with endometriosis or idiopathic infertility. Fertil Steril. 1997;68:826–30.
96. Wentzel P, Eriksson UJ. A diabetes-like environment increases malformation rate and diminishes prostaglandin E(2) in rat embryos: reversal by administration of vitamin E and folic acid. Birth Defects Res A Clin Mol Teratol. 2005;73:506–11.
97. Wiktor H, Kankofer M, Schmerold I, Dadak A, Lopucki M, Niedermüller H. Oxidative DNA damage in placentas from normal and pre-eclamptic pregnancies. Virchows Arch. 2004;445:74–8.
98. Yessoufou A, Soulaimann N, Merzouk SA, Moutairou K, Ahissou H, Prost J, et al. N-3 fatty acids modulate antioxidant status in diabetic rats and their macrosomic offspring. Int J Obes (Lond). 2006;30:739–50.