Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-29T00:54:40.587Z Has data issue: false hasContentIssue false

Factors related to follicular oxidative stress in intracytoplasmic sperm injection cycles and its effects on granulosa cells

Published online by Cambridge University Press:  28 September 2020

Seda Karabulut*
Affiliation:
Istanbul Medipol University, International School of Medicine, Histology and Embryology Department, Istanbul, Turkey Istanbul Medipol University, REMER Center, Istanbul, Turkey
Oya Korkmaz
Affiliation:
Istanbul Medipol University, International School of Medicine, Histology and Embryology Department, Istanbul, Turkey Istanbul Medipol University, REMER Center, Istanbul, Turkey
Pelin Kutlu
Affiliation:
Medicana Çamlıca Hospital, IVF Center, Istanbul, Turkey
Ilknur Keskin
Affiliation:
Istanbul Medipol University, International School of Medicine, Histology and Embryology Department, Istanbul, Turkey Istanbul Medipol University, REMER Center, Istanbul, Turkey
*
Author for correspondence: Seda Karabulut. Istanbul Medipol University, International School of Medicine, Department of Histology and Embryology, Kavacık Neighborhood, 19 Ekinciler Street, Beykoz, Istanbul, Turkey. Tel: +90 532 273 98 64. E-mail: [email protected]

Summary

The aim of the present study was to investigate several common conditions that may potentially be correlated with follicular oxidative status during an intracytoplasmic sperm injection (ICSI) cycle and that include the serum oestrogen level on the day of oocyte pick-up, maternal age and pregnancy outcome. Patients that were enrolled in the study were classified randomly into three groups using their numerical order. The first group were classified based on maternal age (<35 and ≥35 years) (n = 398), the second group on the serum oestradiol (E2) level on the day of human chorionic gonadotropin (hCG) administration (levels >90th percentile and ≤ 90th percentile) (n = 491) and the third group on pregnancy outcome (positive/negative) (n = 376). The groups were matched for the other variables (stimulation protocol, dose of gonadotropin, duration of stimulation, antral follicle count, body mass index, basal follicle stimulating hormone (FSH), and E2 levels and day of hCG trigger) to prevent the possible contribution of those parameters to the results. Each group was matched for other variables (stimulation protocol, dose of gonadotrophin, duration of stimulation, antral follicle count, body mass index, basal FSH and E2 levels and day of hCG trigger) that may have affected the outcome, except for the parameter under investigation. Maternal age (P = 0.044,168 r = 0.418), oestrogen level on day of hCG administration (P = 0.001, r = 0.436) and pregnancy outcome (AUC = 0.65, P = 0.071) were found to be correlated with follicular oxidative status. The results obtained will help us to shield patients from possible situations that may cause oxidative stress and therefore adverse outcomes of an ICSI cycle.

Type
Research Article
Copyright
© The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agarwal, A and Allamaneni, SS (2011). Free radicals and male reproduction. J Indian Med Assoc 109, 184–7.Google ScholarPubMed
Agarwal, A, Aponte-Mellado, A, Premkumar, BJ, Shaman, A and Gupta, S (2012). The effects of oxidative stress on female reproduction: a review. Reprod Biol Endocrinol 10, 49.CrossRefGoogle ScholarPubMed
Appasamy, M, Jauniaux, E, Serhal, P, Al-Qahtani, A, Groome, NP and Muttukrishna, S (2008). Evaluation of the relationship between follicular fluid oxidative stress, ovarian hormones, and response to gonadotropin stimulation. Fertil Steril 89, 912–21.10.1016/j.fertnstert.2007.04.034CrossRefGoogle ScholarPubMed
Aurrekoetxea, I, Ruiz-Sanz, JI, del Agua, AR, Navarro, R, Hernández, ML, Matorras, R, Prieto, B and Ruiz-Larrea, MB (2010). Serum oxidizability and antioxidant status in patients undergoing in vitro fertilization. Fertil Steril 94, 1279–86.CrossRefGoogle ScholarPubMed
Bedaiwy, MA, Elnashar, SA, Goldberg, JM, Sharma, R, Mascha, EJ, Arrigain, S, Agarwal, A and Falcone, T (2012). Effect of follicular fluid oxidative stress parameters on intracytoplasmic sperm injection outcome. Gynecol Endocrinol 28, 51–5.CrossRefGoogle ScholarPubMed
Borowiecka, M, Wojsiat, J, Polac, I, Radwan, M, Radwan, P and Zbikowska, HM (2012). Oxidative stress markers in follicular fluid of women undergoing in vitro fertilization and embryo transfer. Syst Biol Reprod Med 58, 301–5.10.3109/19396368.2012.701367CrossRefGoogle ScholarPubMed
Calhoun, KC, Barnhart, KT, Elovitz, MA and Srinivas, SK (2011). Evaluating the association between assisted conception and the severity of preeclampsia. ISRN Obstet Gynecol 2011, 928592.CrossRefGoogle ScholarPubMed
Celik, E, Celik, O, Kumbak, B, Yilmaz, E, Turkcuoglu, I, Simsek, Y, Karaer, A, Minareci, Y, Ozerol, E and Tanbek, K (2012). A comparative study on oxidative and antioxidative markers of serum and follicular fluid in GnRH agonist and antagonist cycles. J Assist Reprod Genet 29, 1175–83.CrossRefGoogle ScholarPubMed
Da Broi, MG, Giorgi, VSI, Wang, F, Keefe, DL, Albertini, D and Navarro, PA (2018). Influence of follicular fluid and cumulus cells on oocyte quality: clinical implications. J Assist Reprod Genet 35, 735–51.CrossRefGoogle ScholarPubMed
Erel, O (2004). A novel automated method to measure total antioxidant response against potent free radical reactions. Clin Biochem 37, 112–9.CrossRefGoogle ScholarPubMed
Erel, O (2005). A new automated colorimetric method for measuring total oxidant status. Clin Biochem 38, 1103–11.10.1016/j.clinbiochem.2005.08.008CrossRefGoogle ScholarPubMed
Farhi, J, Ben-Haroush, A, Andrawus, N, Pinkas, H, Sapir, O, Fisch, B and Ashkenazi, J (2010). High serum oestradiol concentrations in IVF cycles increase the risk of pregnancy complications related to abnormal placentation. Reprod Biomed Online 21, 331–7.10.1016/j.rbmo.2010.04.022CrossRefGoogle ScholarPubMed
Fissore, RA, Kurokawa, M, Knott, J, Zhang, M and Smyth, J (2002). Mechanisms underlying oocyte activation and postovulatory ageing. Reproduction 124, 745–54.10.1530/rep.0.1240745CrossRefGoogle ScholarPubMed
Fujimoto, VY, Bloom, MS, Huddleston, HG, Shelley, WB, Ocque, AJ and Browne, RW (2011). Correlations of follicular fluid oxidative stress biomarkers and enzyme activities with embryo morphology parameters during in vitro fertilization. Fertil Steril 96, 1357–61.10.1016/j.fertnstert.2011.09.032CrossRefGoogle ScholarPubMed
Gupta, S, Ghulmiyyah, J, Sharma, R, Halabi, J and Agarwal, A (2014). Power of proteomics in linking oxidative stress and female infertility. Biomed Res Int 2014, 916212.CrossRefGoogle ScholarPubMed
Imudia, AN, Awonuga, AO, Doyle, JO, Kaimal, AJ, Wright, DL, Toth, TL and Styer, AK (2012). Peak serum estradiol level during controlled ovarian hyperstimulation is associated with increased risk of small for gestational age and preeclampsia in singleton pregnancies after in vitro fertilization. Fertil Steril 97, 1374–9.CrossRefGoogle ScholarPubMed
Janowski, D, Salilew-Wondim, D, Torner, H, Tesfaye, D, Ghanem, N, Tomek, W, El-Sayed, A, Schellander, K and Hölker, M (2012). Incidence of apoptosis and transcript abundance in bovine follicular cells is associated with the quality of the enclosed oocyte. Theriogenology 78, 656–69.CrossRefGoogle ScholarPubMed
Klinkert, ER (2005). Clinical significance and management of poor response in IVF. Thesis Utrecht University, ISBN-10: 9090198733.Google Scholar
Kryston, TB, Georgiev, AB, Pissis, P and Georgakilas, AG (2011). Role of oxidative stress and DNA damage in human carcinogenesis. Mutat Res 711, 193201.10.1016/j.mrfmmm.2010.12.016CrossRefGoogle ScholarPubMed
Lord, T and Aitken, RJ (2013). Oxidative stress and ageing of the post-ovulatory oocyte. Reproduction 21, 146, R21727.10.1530/REP-13-0111CrossRefGoogle Scholar
Luddi, A, Capaldo, A, Focarelli, R, Gori, M, Morgante, G, Piomboni, P and De-Leó, V (2016). Antioxidants reduce oxidative stress in follicular fluid of aged women undergoing IVF. Reprod Biol Endocrinol 14, 57.10.1186/s12958-016-0184-7CrossRefGoogle ScholarPubMed
Matos, L, Stevenson, D, Gomes, F, Silva-Carvalho, JL and Almeida, H (2009). Superoxide dismutase expression in human cumulus oophorus cells. Mol Hum Reprod 15, 411–9.CrossRefGoogle ScholarPubMed
Miao, YL, Kikuchi, K, Sun, QY and Schatten, H (2009). Oocyte aging: cellular and molecular changes, developmental potential and reversal possibility. Hum Reprod Update 15, 573–85.10.1093/humupd/dmp014CrossRefGoogle ScholarPubMed
Neri, M, Fineschi, V, Di-Paolo, M, Pomara, C, Riezzo, I, Turillazzi, E and Cerretani, D (2015). Cardiac oxidative stress and inflammatory cytokines response after myocardial infarction. Curr Vasc Pharmacol 3, 2636.10.2174/15701611113119990003CrossRefGoogle Scholar
Newsholme, P, Cruzat, VF, Keane, KN, Carlessi R and de Bittencourt PI Jr (2016). Molecular mechanisms of ROS production and oxidative stress in diabetes. Biochem J 473, 4527–50.CrossRefGoogle ScholarPubMed
Okyay, AG, Aslan, M, Taşkın, A, Selek, S, Cengiz-Altın, G and Kahraman, S (2014). Oxidative stress markers in IVF patients and their association with pregnancy results. Turkiye Klinikleri J Med Sci 34, 204–9.10.5336/medsci.2013-36880CrossRefGoogle Scholar
Oyawoye, O, Abdel-Gadir, A, Garner, A, Constantinovici, N, Perrett, C and Hardiman, P (2003). Antioxidants and reactive oxygen species in follicular fluid of women undergoing IVF: relationship to outcome. Hum Reprod 18, 2270–4.10.1093/humrep/deg450CrossRefGoogle Scholar
Pacella, L, Zander-Fox, DL, Armstrong, DT and Lane, M (2012). Women with reduced ovarian reserve or advanced maternal age have an altered follicular environment. Fertil Steril 98, 986–94.10.1016/j.fertnstert.2012.06.025CrossRefGoogle ScholarPubMed
Palini, S, Benedetti, S, Tagliamonte, MC, De-Stefani, S, Primiterra, M, Polli, V, Rocchi, P, Catalani, S, Battistelli, S, Canestrari, F and Bulletti, C (2014). Influence of ovarian stimulation for IVF/ICSI on the antioxidant defence system and relationship to outcome. Reprod Biomed Online 29, 6571.10.1016/j.rbmo.2014.03.010CrossRefGoogle Scholar
Pasqualotto, EB, Agarwal, A, Sharma, RK, Izzo, VM, Pinotti, JA, Joshi, NJ and Rose, BI (2004). Effect of oxidative stress in follicular fluid on the outcome of assisted reproductive procedures. Fertil Steril 81, 973–6.10.1016/j.fertnstert.2003.11.021CrossRefGoogle ScholarPubMed
Pereira, AC and Martel, F (2014). Oxidative stress in pregnancy and fertility pathologies. Cell Biol Toxicol 30, 301–12.10.1007/s10565-014-9285-2CrossRefGoogle ScholarPubMed
Radi, E, Formichi, P, Battisti, C and Federico, A (2014). Apoptosis and oxidative stress in neurodegenerative diseases. J Alzheimers Dis 42(Suppl 3), S12552.CrossRefGoogle ScholarPubMed
Revelli, A, Delle-Piane, L, Casano, S, Molinari, E, Massobrio, M and Rinaudo, P (2009). Follicular fluid content and oocyte quality: from single biochemical markers to metabolomics. Reprod Biol Endocrinol 7, 40.10.1186/1477-7827-7-40CrossRefGoogle ScholarPubMed
Rice, S, Christoforidis, N, Gadd, C, Nikolaou, D, Seyani, L, Donaldson, A, Margara, R, Hardy, K and Franks, S (2005). Impaired insulin-dependent glucose metabolism in granulosa-lutein cells from anovulatory women with polycystic ovaries. Hum Reprod 20, 373–81.CrossRefGoogle ScholarPubMed
Rotterdam ESHRE/ASRM-Sponsored PCOS Consensus Workshop Group (2004). Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome. Fertil Steril 81, 1925.10.1016/j.fertnstert.2003.10.004CrossRefGoogle Scholar
Ruder, EH, Hartman, TJ and Goldman, MB (2009). Impact of oxidative stress on female fertility. Curr Opin Obstet Gynecol 21, 219–22.CrossRefGoogle ScholarPubMed
Sikka, SC (2004). Role of oxidative stress and antioxidants in andrology and assisted reproductive technology. J Androl 25, 518.10.1002/j.1939-4640.2004.tb02751.xCrossRefGoogle ScholarPubMed
Smits, RM, Mackenzie-Proctor, R, Fleischer, K and Showell, MG (2018). Antioxidants in fertility: effect on male and female reproductive outcomes. Fertil Steril 110, 578–80.10.1016/j.fertnstert.2018.05.028CrossRefGoogle Scholar
Takahashi, T, Takahashi, E, Igarashi, H, Tezuka, N and Kurachi, H (2003). Impact of oxidative stress in aged mouse oocytes on calcium oscillations at fertilization. Mol Reprod Dev 66, 143–52.CrossRefGoogle ScholarPubMed
Tarín, JJ (1996). Potential effects of age-associated oxidative stress on mammalian oocytes/embryos. Mol Hum Reprod 2, 717–24.10.1093/molehr/2.10.717CrossRefGoogle ScholarPubMed
Tatemoto, H, Sakurai, N and Muto, N (2000). Protection of porcine oocytes against apoptotic cell death caused by oxidative stress during In vitro maturation: role of cumulus cells. Biol Reprod 63, 805–10.10.1095/biolreprod63.3.805CrossRefGoogle ScholarPubMed
Tatemoto, H, Muto, N, Sunagawa, I, Shinjo, A and Nakada, T (2004). Protection of porcine oocytes against cell damage caused by oxidative stress during in vitro maturation: role of superoxide dismutase activity in porcine follicular fluid. Biol Reprod 71, 1150–7.CrossRefGoogle ScholarPubMed
Thouas, GA, Trounson, AO and Jones, GM (2005). Effect of female age on mouse oocyte developmental competence following mitochondrial injury. Biol Reprod 73, 366–73.CrossRefGoogle ScholarPubMed
Zhang, L, Fujii, S and Kosaka, H (2007). Effect of oestrogen on reactive oxygen species production in the aortas of ovariectomized Dahl salt sensitive rats. J Hypertens 25, 407–14.10.1097/HJH.0b013e328010beeeCrossRefGoogle ScholarPubMed