Abstract
Endometriosis, a highly prevalent gynecological disease, is often associated with infertility, even in its milder forms (minimal and mild endometriosis). However, no consensus has been established with regard to this relationship and the possible mechanisms involved have not been completely elucidated. The oocyte is believed to have an important role in the infertility presented by these patients. Hence, oxidative stress events associated with alterations in the peritoneal, serum and/or follicular microenvironments might result in poor oocyte quality and compromise the reproductive potential of these women. Here, we review possible mechanisms involved in oocyte quality impairment that might lead to infertility in patients with early endometriosis.
Similar content being viewed by others
References
Agarwal A, Saleh RA, Bedaiwy MA (2003) Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil Steril 79:829–843
Agarwal A, Gupta S, Sharma RK (2005) Role of oxidative stress in female reproduction. Reprod Biol Endocrinol 3:28
Akande VA, Hunt LP, Cahill DJ, Jenkins JM (2004) Differences in time to natural conception between women with unexplained infertility and infertile women with minor endometriosis. Hum Reprod 19:96–103
Albertini DF (1992) Cytoplasmic microtubular dynamics and chromatin organization during mammalian oogenesis and oocyte maturation. Mutat Res 296:57–68
Al-Fadhli R, Kelly SM, Tulandi T, Tanr SL (2006) Effects of different stages of endometriosis on the outcome of in vitro fertilization. J Obstet Gynaecol Can 28:888–891
Alpay Z, Saed GM, Diamond MP (2006) Female infertility and free radicals: potential role in adhesions and endometriosis. J Soc Gynecol Investig 13:390–398
Appasamy M, Jauniaux E, Serhal P, Al-Qahtani A, Groome NP, Muttukrishna S (2008) Evaluation of the relationship between follicular fluid oxidative stress, ovarian hormones, and response to gonadotropin stimulation. Fertil Steril 89:912–921
Attaran M, Pasqualotto E, Falcone T, Goldberg JM, Miller KF, Agarwal A, Sharma RK (2000) The effect of follicular fluid reactive oxygen species on the outcome of in vitro fertilization. Int J Fertil Womens Med 45:314–320
Augoulea A, Alexandrou A, Creatsa M, Vrachnis N, Lambrinoudaki I (2012) Pathogenesis of endometriosis: the role of genetics, inflammation and oxidative stress. Arch Gynecol Obstet 286:99–103
Barcelos ID, Vieira RC, Ferreira EM, Martins WP, Ferriani RA, Navarro PA (2009) Comparative analysis of the spindle and chromosome configurations of in vitro-matured oocytes from patients with endometriosis and from control subjects: a pilot study. Fertil Steril 92:1749–1752
Barcelos ID, Donabella FC, Ribas CP, Meola J, Ferriani RA, Paz CC de, Navarro PA (2015) Down-regulation of the CYP19A1 gene in cumulus cells of infertile women with endometriosis. Reprod Biomed Online 30:532–541
Bellelis P, Dias JA Jr, Podgaec S, Gonzales M, Baracat EC, Abrao MS (2010) Epidemiological and clinical aspects of pelvic endometriosis—a case series. Rev Assoc Med Bras 56:467–471
Bergqvist A, D’Hooghe T (2002) Mini symposium on pathogenesis of endometriosis and treatment of endometriosis-associated subfertility. Introduction: the endometriosis enigma. Hum Reprod Update 8:79–83
Brizek CL, Schlaff S, Pellegrini VA, Frank JB, Worrilow KC (1995) Increased incidence of aberrant morphological phenotypes in human embryogenesis—an association with endometriosis. J Assist Reprod Genet 12:106–112
Campos Petean C, Ferriani RA, Reis RM dos, Moura MD de, Jordao AA Jr, Navarro PA (2008) 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 90:2080–2085
Carvalho LF, Samadder AN, Agarwal A, Fernandes LF, Abrao MS (2012) Oxidative stress biomarkers in patients with endometriosis: systematic review. Arch Gynecol Obstet 286:1033–1040
Da Broi MG, Andrade AZ, Rodrigues JK, Paz CCP, Jordão AA, Navarro PA (2013) Total antioxidant capacity (TAC) levels in follicular fluid of infertile patients undergoing ICSI: a possible predictor of clinical pregnancy. IFFS/ASRM Conjoint Meeting. Fertil Steril 100:S425
Da Broi MG, Albuquerque FO, Andrade AZ de, Cardoso RL, Jordão AA Jr, Navarro PA (2014a) Systemic and follicular oxidative stress in infertile women with endometriosis undergoing controlled ovarian stimulation for ICSI: is there a role in the ethiopathogenesis of infertility? Fertil Steril 102:e79
Da Broi MG, Malvezzi H, Paz CC, Ferriani RA, Navarro PA (2014b) Follicular fluid from infertile women with mild endometriosis may compromise the meiotic spindles of bovine metaphase II oocytes. Hum Reprod 29:315–323
Da Broi MG, Rodrigues JK, Andrade AZ, Giorgi VSI, Jordão AA, Navarro P (2014c) Systemic and follicular oxidative stress in infertile women with minimal/mild endometriosis undergoing controlled ovarian stimulation for ICSI: is there a role in the etiopathogenesis of infertility? JBRA Assist Reprod 18:117
De Santis L, Cino I, Rabellotti E, Calzi F, Persico P, Borini A, Coticchio G (2005) Polar body morphology and spindle imaging as predictors of oocyte quality. Reprod Biomed Online 11:36–42
Donabela F, Barcelos I, Pavdovan C, Meola J, Ferriani RA, Navarro P (2011) PTGS2 gene expression (COX2) in cummulus oophorus cells of endometriosis and control infertile patients submitted to ICSI. ASRM 67th Annual Meeting. Fertil Steril 96: S236–S237
Eichenlaub-Ritter U, Shen Y, Tinneberg HR (2002) Manipulation of the oocyte: possible damage to the spindle apparatus. Reprod Biomed Online 5:117–124
Eppig JJ, Wigglesworth K, Pendola FL (2002) The mammalian oocyte orchestrates the rate of ovarian follicular development. Proc Natl Acad Sci U S A 99:2890–2894
Ferreira EM, Vireque AA, Adona PR, Meirelles FV, Ferriani RA, Navarro PA (2009) Cytoplasmic maturation of bovine oocytes: structural and biochemical modifications and acquisition of developmental competence. Theriogenology 71:836–848
Ferriani RA, Barcelos I, Donabela F, Ribas C, Meola J, Navarro PA (2013) Lower expression of the gene CYP19A1 in cumulus oophorus cells from infertile women with minimal and mild endometriosis may be involved in the infertility related to this disease. 5th International IVI Congress, Seville, Spain. http://comtecmed.com/ivi/2013/Uploads/Editor/abstract_41.pdf
Garcia-Velasco JA, Arici A (1999) Is the endometrium or oocyte/embryo affected in endometriosis? Hum Reprod 14(Suppl 2):77–89
Garrido N, Navarro J, Remohi J, Simon C, Pellicer A (2000) Follicular hormonal environment and embryo quality in women with endometriosis. Hum Reprod Update 6:67–74
Giorgi VS, Da Broi MG, Paz CC, Ferriani RA, Navarro PA (2015) N-acetyl-cysteine and L-carnitine prevent meiotic oocyte damage induced by follicular fluid from infertile women with mild endometriosis. Reprod Sci (in press)
Giudice LC, Kao LC (2004) Endometriosis. Lancet 364:1789–1799
Gnoth C, Godehardt D, Godehardt E, Frank-Herrmann P, Freundl G (2003) Time to pregnancy: results of the German prospective study and impact on the management of infertility. Hum Reprod 18:1959–1966
Gupta S, Agarwal A, Krajcir N, Alvarez JG (2006) Role of oxidative stress in endometriosis. Reprod Biomed Online 13:126–134
Gupta S, Goldberg JM, Aziz N, Goldberg E, Krajcir N, Agarwal A (2008) Pathogenic mechanisms in endometriosis-associated infertility. Fertil Steril 90:247–257
Halliwell B (1994) Free radicals, antioxidants, and human disease: curiosity, cause, or consequence? Lancet 344:721–724
Hamel M, Dufort I, Robert C, Gravel C, Leveille MC, Leader A, Sirard MA (2008) Identification of differentially expressed markers in human follicular cells associated with competent oocytes. Hum Reprod 23:1118–1127
Haouzi D, Hamamah S (2009) Pertinence of apoptosis markers for the improvement of in vitro fertilization (IVF). Curr Med Chem 16:1905–1916
Hu Y, Betzendahl I, Cortvrindt R, Smitz J, Eichenlaub-Ritter U (2001) Effects of low O2 and ageing on spindles and chromosomes in mouse oocytes from pre-antral follicle culture. Hum Reprod 16:737–748
Hughes EG, Fedorkow DM, Collins JA (1993) A quantitative overview of controlled trials in endometriosis-associated infertility. Fertil Steril 59:963–970
Jackson LW, Schisterman EF, Dey-Rao R, Browne R, Armstrong D (2005) Oxidative stress and endometriosis. Hum Reprod 20:2014–2020
Jianini BTGM, Giorgi VSI, Malvezzi H, Da Broi MG, Paz CCP da, Navarro PAAS (2014) Peritoneal fluid from infertile women with minimal/mild endometriosis may compromise the spindle of metaphase II bovine oocytes. 8th Annual Congress of the SBRA. JBRA Assist Reprod 18:117–118
Kim NH, Chung HM, Cha KY, Chung KS (1998) Microtubule and microfilament organization in maturing human oocytes. Hum Reprod 13:2217–2222
Kumbak B, Kahraman S, Karlikaya G, Lacin S, Guney A (2008) In vitro fertilization in normoresponder patients with endometriomas: comparison with basal simple ovarian cysts. Gynecol Obstet Invest 65:212–216
Liu L, Trimarchi JR, Navarro P, Blasco MA, Keefe DL (2003) Oxidative stress contributes to arsenic-induced telomere attrition, chromosome instability, and apoptosis. J Biol Chem 278:31998–32004
Ma CH, Yan LY, Qiao J, Sha W, Li L, Chen Y, Sun QY (2010) Effects of tumor necrosis factor-alpha on porcine oocyte meiosis progression, spindle organization, and chromosome alignment. Fertil Steril 93:920–926
Mandelbaum J, Anastasiou O, Levy R, Guerin JF, Larouziere V de, Antoine JM (2004) Effects of cryopreservation on the meiotic spindle of human oocytes. Eur J Obstet Gynecol Reprod Biol 113 (Suppl 1):S17–S23
Mansour G, Abdelrazik H, Sharma RK, Radwan E, Falcone T, Agarwal A (2009) L-carnitine supplementation reduces oocyte cytoskeleton damage and embryo apoptosis induced by incubation in peritoneal fluid from patients with endometriosis. Fertil Steril 91:2079–2086
Marcoux S, Maheux R, Berube S (1997) Laparoscopic surgery in infertile women with minimal or mild endometriosis. Canadian Collaborative Group on Endometriosis. N Engl J Med 337:217–222
Mullen SF, Agca Y, Broermann DC, Jenkins CL, Johnson CA, Critser JK (2004) The effect of osmotic stress on the metaphase II spindle of human oocytes, and the relevance to cryopreservation. Hum Reprod 19:1148–1154
Murphy AA, Santanam N, Morales AJ, Parthasarathy S (1998) Lysophosphatidyl choline, a chemotactic factor for monocytes/T-lymphocytes is elevated in endometriosis. J Clin Endocrinol Metab 83:2110–2113
Navarro PA, Liu L, Keefe DL (2004) In vivo effects of arsenite on meiosis, preimplantation development, and apoptosis in the mouse. Biol Reprod 70:980–985
Navarro PA, Liu L, Ferriani RA, Keefe DL (2006) Arsenite induces aberrations in meiosis that can be prevented by coadministration of N-acetylcysteine in mice. Fertil Steril 85 (Suppl 1):1187–1194
Navarro PA, Malvezzi H, Da Broi MG, Rosa e Silva JC, Vireque AA, Meola J (2013) The peritoneal fluid of infertile women with and without minimal/mild endometriosis reduces the expression of genes GSR and CAT in bovine oocytes. 5th International IVI Congress, Seville, Spain. http://comtecmed.com/ivi/2013/Uploads/Editor/abstract_88.pdf
Ngo C, Chereau C, Nicco C, Weill B, Chapron C, Batteux F (2009) Reactive oxygen species controls endometriosis progression. Am J Pathol 175:225–234
Parazzini F (1999) Ablation of lesions or no treatment in minimal-mild endometriosis in infertile women: a randomized trial. Gruppo Italiano per lo Studio dell’Endometriosi. Hum Reprod 14:1332–1334
Pasqualotto EB, Agarwal A, Sharma RK, Izzo VM, Pinotti JA, Joshi NJ, Rose BI (2004) Effect of oxidative stress in follicular fluid on the outcome of assisted reproductive procedures. Fertil Steril 81:973–976
Pellicer A, Oliveira N, Ruiz A, Remohi J, Simon C (1995) Exploring the mechanism(s) of endometriosis-related infertility: an analysis of embryo development and implantation in assisted reproduction. Hum Reprod 10 (Suppl 2):91–97
Practice Committee of the ASRM (2012) Endometriosis and infertility: a committee opinion. Fertil Steril 98:591–598
Shkolnik K, Tadmor A, Ben-Dor S, Nevo N, Galiani D, Dekel N (2011) Reactive oxygen species are indispensable in ovulation. Proc Natl Acad Sci U S A 108:1462–1467
Signorile PG, Baldi A (2010) Endometriosis: new concepts in the pathogenesis. Int J Biochem Cell Biol 42:778–780
Simon C, Gutierrez A, Vidal A, de los Santos MJ, Tarin JJ, Remohi J, Pellicer A (1994) Outcome of patients with endometriosis in assisted reproduction: results from in-vitro fertilization and oocyte donation. Hum Reprod 9:725–729
Singh N, Lata K, Naha M, Malhotra N, Tiwari A, Vanamail P (2014) Effect of endometriosis on implantation rates when compared to tubal factor in fresh non donor in vitro fertilization cycles. J Hum Reprod Sci 7:143–147
Sung L, Mukherjee T, Takeshige T, Bustillo M, Copperman AB (1997) Endometriosis is not detrimental to embryo implantation in oocyte recipients. J Assist Reprod Genet 14:152–156
Szczepanska M, Kozlik J, Skrzypczak J, Mikolajczyk M (2003) Oxidative stress may be a piece in the endometriosis puzzle. Fertil Steril 79:1288–1293
Tanghe S, Van Soom A, Nauwynck H, Coryn M, Kruif A de (2002) Minireview: functions of the cumulus oophorus during oocyte maturation, ovulation, and fertilization. Mol Reprod Dev 61:414–424
Tesfaye D, Ghanem N, Carter F, Fair T, Sirard MA, Hoelker M, Schellander K, Lonergan P (2009) Gene expression profile of cumulus cells derived from cumulus-oocyte complexes matured either in vivo or in vitro. Reprod Fertil Dev 21:451–461
Van Blerkom J, Davis P (2001) Differential effects of repeated ovarian stimulation on cytoplasmic and spindle organization in metaphase II mouse oocytes matured in vivo and in vitro. Hum Reprod 16:757–764
Van Langendonckt A, Casanas-Roux F, Donnez J (2002) Oxidative stress and peritoneal endometriosis. Fertil Steril 77:861–870
Volarcik K, Sheean L, Goldfarb J, Woods L, Abdul-Karim FW, Hunt P (1998) The meiotic competence of in-vitro matured human oocytes is influenced by donor age: evidence that folliculogenesis is compromised in the reproductively aged ovary. Hum Reprod 13:154–160
Wang WH, Keefe DL (2002) Prediction of chromosome misalignment among in vitro matured human oocytes by spindle imaging with the PolScope. Fertil Steril 78:1077–1081
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Da Broi, M.G., Navarro, P.A. Oxidative stress and oocyte quality: ethiopathogenic mechanisms of minimal/mild endometriosis-related infertility. Cell Tissue Res 364, 1–7 (2016). https://doi.org/10.1007/s00441-015-2339-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00441-015-2339-9