Preeclampsia and level of oxidative stress in the first trimester of pregnancy

Mirjana Bogavac; Ana Jakovljević; Zoran Stajić; Aleksandra Nikolić; Mirjana Milošević-Tošić; Jadranka Dejanović; Zagorka Lozanov-Crvenković

doi:10.2298/VSP150517251B

Mirjana Bogavac Clinical Centre of Vojvodina, Department of Obstetrics and Gynecology, Novi Sad, Serbia; University of Novi Sad, Faculty of Medicine, Novi Sad, Serbia.
Ana Jakovljević University of Novi Sad, Faculty of Medicine, Novi Sad, Serbia; Clinical Centre of Vojvodina, Centre for Laboratory Medicine, Novi Sad, Serbia.
Zoran Stajić Institute for Health Protection of the Ministry of Interior, Department of Internal Medicine, §Division of Cardiology, Belgrade, Serbia.
Aleksandra Nikolić University of Novi Sad, Faculty of Medicine, Novi Sad, Serbia; Clinical Centre of Vojvodina, Emergency Centre, Novi Sad, Serbia.
Mirjana Milošević-Tošić University of Novi Sad, Faculty of Medicine, Novi Sad, Serbia; University of Novi Sad, Faculty of Science, Novi Sad, Serbia.
Jadranka Dejanović University of Novi Sad, Faculty of Medicine, Novi Sad, Serbia; Institute for Cardiovascular Diseases, **Clinic of Cardiology, Sremska Kamenica, Serbia
Zagorka Lozanov-Crvenković University of Novi Sad, Faculty of Medicine, Novi Sad, Serbia; University of Novi Sad, Faculty of Science, Novi Sad, Serbia.

DOI: https://doi.org/10.2298/VSP150517251B

Keywords: pregnancy complications, pre-eclampsia, oxidative stress, superoxide dismutase, glutathione peroxidase, sensitivity and specificity,

Abstract

Background/Aim. Preeclampsia (PE) is a multisystemic syndrome that complicates 5–8% of all pregnancies. The aim of this study was to evaluate the biochemical parameters of oxidative stress in the first trimester of pregnancy in patients with preeclampsia, with the purpose of comparing the level of oxidative stress with normal pregnancy. Methods. The study was conducted as a prospective study. It included totally 107 pregnant women divided into two groups. In the study group (n = 33) there were women who developed preeclampsia in the current pregnancy. The control group (n = 74) included healthy pregnant women. Blood samples were taken between 11th and 14th weeks of gestation, and the values of superoxide dismutase (SOD), glutathione peroxidase (GSH-Px) and total antioxidant status (TAS) were determined in serum by enzymatic colorimetric methods. Results. The values of SOD and GHS-Px were statistically higher in the study group, while the values of TAS were statistically higher in the control group. The level of TAS inversely correlated with GSH-Px and SOD, but there is no statistically significant correlation between GSH-Px and SOD in the study group. Conclusion. The results of this study suggest a higher level of oxidative stress in the first trimester of pregnancy with preeclampsia, which may indicate that the initiation and development of pathophysiological processes underlying preeclampsia start much earlier than the clinical syndrome exhibit.

Author Biographies

Mirjana Bogavac, Clinical Centre of Vojvodina, Department of Obstetrics and Gynecology, Novi Sad, Serbia; University of Novi Sad, Faculty of Medicine, Novi Sad, Serbia.

Department of Obstetrics and Gynecology

Specialist O&G

Ana Jakovljević, University of Novi Sad, Faculty of Medicine, Novi Sad, Serbia; Clinical Centre of Vojvodina, Centre for Laboratory Medicine, Novi Sad, Serbia.

Centre for Laboratory Medicine

Specialist of Biomedical Chemistry

Zoran Stajić, Institute for Health Protection of the Ministry of Interior, Department of Internal Medicine, §Division of Cardiology, Belgrade, Serbia.

Department of Internal Medicine

Specialist of Internal Medicine

Aleksandra Nikolić, University of Novi Sad, Faculty of Medicine, Novi Sad, Serbia; Clinical Centre of Vojvodina, Emergency Centre, Novi Sad, Serbia.

Emergency Center, Urgent Laboratory at Department of Obstetrics and Gynecology

Specialist of Biomedical Chemistry

Mirjana Milošević-Tošić, University of Novi Sad, Faculty of Medicine, Novi Sad, Serbia; University of Novi Sad, Faculty of Science, Novi Sad, Serbia.

Emergency Center, Urgent Laboratory at Department of Obstetrics and Gynecology

Specialist of Biomedical Chemistry

Jadranka Dejanović, University of Novi Sad, Faculty of Medicine, Novi Sad, Serbia; Institute for Cardiovascular Diseases, **Clinic of Cardiology, Sremska Kamenica, Serbia

Institute for Cardiovascular Diseases Sremska Kamenica, Clinic of Cardiology, Sremska Kamenica

Zagorka Lozanov-Crvenković, University of Novi Sad, Faculty of Medicine, Novi Sad, Serbia; University of Novi Sad, Faculty of Science, Novi Sad, Serbia.

Department of Mathematics and Informatics

Informatics specialistt

References

Kambayashi Y, Tero-Kubota S, Yamamoto Y, Kato M, Nakano M, Yagi K, et al. Formation of superoxide anion during ferrous ion-induced decomposition of linoleic acid hydroperoxide un-der aerobic conditions. J Biochem 2003; 134(6): 903−9.

Gupta S, Malhotra N, Sharma D, Chandra A, Agarwal A. Oxida-tive stress and role in female infertility and assisted reproduc-tion: clinical implications. Int J Fertil Steril 2009; 2: 147−64.

Kashinakunti SV, Sunitha H, Gurupadappa K, Shankarprasad DS, Suryaprakash G, Ingin JB. Lipid Peroxidation and Antioxidant Status in Preeclampsia. Al Ameen J Med Sci 2010; 3(1): 38−41.

Djukic MM. Oxidative stress-free radicals, prooxidants and an-tioxidants. Belgrade: Mono i Manjana; 2008. (Serbian)

Halliwell B, Gutteridge JM. Free radicals in biology and medicine. 3rd ed. New York: Oxford University Press Inc; 1999.

Bogavac M, Lakic N, Simin N, Nikolic A, Sudji J, Bozin B. Bacterial vaginosis and biomarkers of oxidative stress in amniotic fluid. J Matern Fetal Neonatal Med 2012; 25(7): 1050−4.

Ruder EH, Hartman TJ, Goldman MB. Impact of oxidative stress on female fertility. Curr Opin Obstet Gynecol 2009; 21(3): 219−22.

Al-Gubory KH, Fowler PA, Garrel C. The roles of cellular reac-tive oxygen species, oxidative stress and antioxidants in preg-nancy outcomes. Int J Biochem Cell Biol 2010; 42(10): 1634−50.

Koruk M, Taysi S, Savas CM, Yilmaz O, Akcay F, Karakok M. Oxidative stress and enzymatic antioxidant status in patients with nonalcoholic steatohepatitis. Ann Clin Lab Sci 2004; 34(1): 57−62.

Suresh DR, Annam V, Pratibha K, Prasad BV. Total antioxidant capacity: A novel early biochemical marker of oxidative stress in HIV infected individuals. J Biomed Sci 2009; 16(1): 61.

Jauniaux E, Watson AL, Hempstock J, Bao YP, Skepper JN, Burton GJ. Onset of maternal arterial blood flow and placental oxida-tive stress. A possible factor in human early pregnancy failure. Am J Pathol 2000; 157(6): 2111−22.

Perrone S, Longini M, Bellieni CV, Centini G, Kenanidis A, De Marco L, et al. Early oxidative stress in amniotic fluid of pregnancies with Down syndrome. Clin Biochem 2007; 40(3−4): 177−80.

Chamy VM, Lepe J, Catalán A, Retamal D, Escobar JA, Madrid EM. Oxidative stress is closely related to clinical severity of pre-eclampsia. Biol Res 2006; 39(2): 229−36.

Palmieri B, Sblendorio V. Oxidative stress tests: Overview on re-liability and use. Part II. Eur Rev Med Pharmacol Sci 2007; 11(6): 383−99.

Gupta S, Agarwal A, Banerjee J, Alvarez JG. The role of oxidative stress in spontaneous abortion and recurrent pregnancy loss: A systematic review. Obstet Gynecol Surv 2007; 62(5): 335−47; quiz 353−4.

Jakovljevic B, Novakov-Mikic A, Brkic S, Bogavac M, Tomic S, Miler V. Lipid peroxidation in the first trimester of pregnancy J Ma-tern Fetal Neonatal Med 2012; 25(8): 1316−8.

Hutcheon JA, Lisonkova S, Joseph KS. Epidemiology of pre-eclampsia and the other hypertensive disorders of pregnancy. Best Pract Res Clin Obstet Gynaecol 2011; 25(4): 391−403.

Ferrazzani S, Luciano R, Garofalo S, Andrea VD, Carolis SD, Ca-rolis MP, et al. Neonatal outcome in hypertensive disorders of pregnancy. Early Hum Dev 2011; 87(6) 445−9.

Gaillard R, Arends LR, Steegers EA, Hofman A, Jaddoe VW. Second- and third-trimester placental hemodynamics and the risks of pregnancy complications: The Generation R Study. Am J Epidemiol 2013; 177(8): 743−54.

Wallis AB, Saftlas AF, Hsia J, Atrash HK. Secular trends in the rates of preeclampsia, eclampsia, and gestational hypertension, United States, 1987-2004. Am J Hypertens 2008; 21(5): 521−6.

Lei Q, Lv LJ, Zhang BY, Wen JY, Liu GC, Lin XH, et al. Ante-partum and post-partum markers of metabolic syndrome in pre-eclampsia. J Hum Hypertens 2011; 25(1): 11−7.

Ministry of Health of the Republic Serbia. Guideline for Diag-nostics and Treatment of lipid Disorders. Available from: http://www.azus.gov.rs/wp-content/uploads/2011/04/ (Serbian)

Ministry of Health of the Republic of Serbia. National Guide-line of good Clinical Practice – Diabetes Mellius. Available from: http//www.minzdravlja.info/downloads/2008/Sa%20Zdravlja/dokumenta/Vodici/diabetes.pdf (Serbian)

Paglia DE, Valentine WN. Studies on the quantitative and qua-litative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 1967; 70(1): 158−69.

Arthur JR, Boyne R. Superoxide dismutase and glutathione pe-roxidase activities in neutrophils from selenium deficient and copper deficient cattle. Life Sci 1985; 36(16): 1569−75.

Erel O. A novel automated direct measurement method for to-tal antioxidant capacity using a new generation, more stable ABTS radical cation. Clin Biochem 2004; 37(4): 277−85.

Yang X, Guo L, Li H, Chen X, Tong X. Analysis of the original causes of placental oxidative stress in normal pregnancy and pre-eclampsia: a hypothesis. J Matern Fetal Neonatal Med 2012; 25(7): 884−8.

George EM, Granger JP. Endothelin: key mediator of hyperten-sion in preeclampsia. Am J Hypertens 2011; 24(9): 964−9.

Rosta K, Molvarec A, Enzsöly A, Nagy B, Rónai Z, Fekete A, et al. Association of extracellular superoxide dismutase (SOD3) Ala40Thr gene polymorphism with pre-eclampsia complicated by severe fetal growth restriction. Eur J Obstet Gynecol Re-prod Biol 2009; 142(2): 134−8.

Sharma JB, Sharma A, Bahadur A, Vimala N, Satyam A, Mittal S. Oxidative stress markers and antioxidant levels in normal pregnancy and pre-eclampsia. Int J Gynaecol Obstet 2006; 94(1): 23−7.

Wruck CJ, Huppertz B, Bose P, Brandenburg L, Pufe T, Kadyrov M. Role of a fetal defence mechanism against oxidative stress in the aetiology of preeclampsia. Histopathology 2009; 55(1): 102−6.

Genc H, Uzun H, Benian A, Simsek G, Gelisgen R, Madazli R, et al. Evaluation of oxidative stress markers in first trimester for assessment of preeclampsia risk. Arch Gynecol Obstet 2011; 284(6): 1367−73.

Hansson SR, Nääv Å, Erlandsson L. Oxidative stress in preec-lampsia and the role of free fetal hemoglobin. Front Physiol 2015; 5: 516.

Lissette C, Prada CE, Medina C, Lopez M. Endothelial dysfunc-tion and preeclampsia: Role of oxidative stress. Front Physiol 2014; 5: 372.

Llurba E, Gratacós E, Martín-Gallán P, Cabero L, Dominguez C. A comprehensive study of oxidative stress and antioxidant status in preeclampsia and normal pregnancy. Free Radic Biol Med 2004; 37(4): 557−70.

Cunninghm FG, Lenevo KJ, Bloom SL, Hauth JC, Rouse DJ, Spong CY. Pregnancy hypertension (Chapter 34). In: Cunninghm FG, Lenevo KJ, Bloom SL, Hauth JC, Rouse DJ, Spong CY, editors. Williams Obstretics. 23rd ed. New York: McGraw-Hill; 2010. p. 706−56.

Vanderlelie J, Scott R, Shibl R, Lewkowicz J, Perkins A, Scuffham PA. First trimester multivitamin/mineral use is associated with reduced risk of pre-eclampsia among overweight and obese women. Matern Child Nutr 2014; doi: 10.1111/mcn.12133. (In Press).