Artificial oocyte activation and intracytoplasmic sperm injection

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1 Artificial oocyte activation and intracytoplasmic sperm injection Mohammad Hossein Nasr-Esfahani, Ph.D., a,b Mohammad Reza Deemeh, M.Sc., a,b and Marziyeh Tavalaee, M.Sc. b a Isfahan Fertility and Infertility Center, Isfahan; and b Andrology and Embryology Department, Reproductive Medicine Research Center, Royan Institute (Isfahan Campus), ACECR, Tehran, Iran Objective: To review different methods for artificial oocyte activation and its impact on intracytoplasmic sperm injection (ICSI). Design: Literature review. Setting: University-based and university-affiliated medical centers. Patient(s): None. Intervention(s): None. Main Outcome Measure(s): None. Result(s): The ICSI procedure improves rates in cases of male factor infertility; however, failure still occurs in 2% to 3% of ICSI cycles. The main cause of failed is failure to complete oocyte activation. The investigators do not use a variety of mechanical, electrical, and chemical methods to mimic the calcium rise necessary to activate oocytes after ICSI. Chemical activation is the most commonly used method for artificial oocyte activation, resulting in high rates. Conclusion(s): Artificial oocyte activation (AOA) may be useful in selected patients who have low potential. Further studies are required to establish the biosafety of AOA, and clinical tests are needed to evaluate the activation potential of semen samples for proper patient selection. (Fertil Steril Ò 2010;94: Ó2010 by American Society for Reproductive Medicine.) Key Words: Artificial oocyte activation, chemical activation, electrical activation, failed, ICSI Assisted reproductive techniques are now responsible for up to 7% of births in some developed countries (1). In vitro (IVF) offers the possibility for to infertile couples, but this technique is not effective for severe male factor infertility. In these patients, sperm cannot penetrate the zona pellucida, so the intracytoplasmic sperm injection (ICSI) technique has been implemented to overcome this problem (2). During this procedure, sperm is directly inseminated into the oocyte. This method is the preferred treatment option for severe male factor infertility. The average normal rate in ICSI is approximately 70%, but total failure still occurs in 2% to 3% of ICSI cycles (3). The literature reveals failure after ICSI may be explained by defects in oocyte, sperm, or the ICSI procedure. Oocyte immaturity or inherited genetic defects may account for failed related to oocyte factors (4). Expulsion of the injected sperm from the oocytes accounts for up to 20% of unfertilized post-icsi oocytes. Viability, abnormal chromatin status, inability of sperm nucleus to decondense, or inability of sperm to activate Received December 6, 2008; revised February 23, 2009; accepted March 14, 2009; published online April 25, M.H.N. has nothing to disclose. M.R.D. has nothing to disclose. M.T. has nothing to disclose. Reprint requests: Mohammad H. Nasr-Esfahani, Ph.D., Andrology and Embryology Department, Reproductive Medicine Research Center, Royan Institute, (Isfahan campus), ACECR, Tehran, Iran (FAX: þ98þ311þ ; mh_nasr@med.mui.ac.ir). oocytes are sperm defects that may account for failed after ICSI (5 11). Indeed, analysis of failed fertilized oocytes after ICSI has revealed that more than 80% of unfertilized oocytes are arrested at the metaphase II (MII) stage, possibly due to failed oocyte activation (12). Although vigorous oocyte aspiration is recommended to increase activation (13), this procedure by itself may not be sufficient for oocyte activation in humans. Therefore, a variety of studies have tried to overcome failure through various methods of artificially activating oocytes after ICSI, including chemical and electrical oocyte activation. Our review discusses the mechanisms of oocyte activation, the different artificial oocyte activation (AOA) procedures available, and their effect on ICSI outcomes. BRIEF OVERVIEW ON MECHANISMS OF OOCYTE ACTIVATION IN THE HUMAN OOCYTE Oocyte activation includes a large number of well-defined morphologic and biochemical end points, some of them occurring within seconds or minutes of sperm oocyte plasma membrane interaction, some occurring over the course of several hours (14). A human oocyte enters the first meiotic division during embryonic life and arrests in this phase for an extended time. Upon resumption of the first meiotic division, the oocyte is subsequently arrested at the second metaphase 520 Fertility and Sterility â Vol. 94, No. 2, July /$36.00 Copyright ª2010 American Society for Reproductive Medicine, Published by Elsevier Inc. doi: /j.fertnstert

2 (MII) where it waits for (14). Upon, spermatozoa overcome the second meiosis arrest by inducing a series of cellular events within the oocyte that are essential for normal development, and are collectively called oocyte activation (15). These events include an early intercellular rise in calcium concentration from endoplasmic reticulum stores. This increase occurs 1 to 3 minutes after fusion of the sperm with oolemma, and it originates at the point of sperm entry (16). The first calcium transient rise is followed by a series of shorter calcium transient rises of high amplitude, which are known as calcium oscillation. As progresses, the amplitude and frequency of calcium transient decreases while their duration increases until absolute cessation (17). Induction of calcium oscillations from intracellular stores in the human oocyte is believed to be triggered by inositol trisphosphate, which is catalyzed by sperm-specific phospholipase C named PLCz, present in the perinuclear theca of sperm (18). The induced calcium oscillation leads to resumption of meiosis, decondensation of sperm nucleus, maternal RNA recruitment, formation of male and female pronuclei, initiation of DNA synthesis, and cleavage (14). In addition, the calcium rise induces cortical granule (CG) exocytosis, leading to cortical reaction, which prevents additional sperm from binding and penetrating the zona pellucida (19). It is of interest to note that a single calcium rise is sufficient for oocyte activation, but calcium oscillations in fertilized eggs are believed to regulate not only short-term events such as oocyte activation but also long-term developmental events, early gene expression, and possibly methylation status (20, 21). Indeed, studies have shown that in mice oscillation patterns can be optimized to increase the extent of parthenogenetic development into early fetal stages, some of which have somites and a beating heart (22, 23). Calcium oscillations are also observed after ICSI (12). Intracytoplasmic sperm injection has allowed researchers to obtain more knowledge about events in different stages of such as sperm capacitation, oocyte activation, and cytoplasmic factors involved in transformation of the sperm nucleus into a pronucleus (24). Research in this area suggests that a factor or factors present in the spermatozoa especially in the head region known as PLCz are responsible for induced calcium oscillation and subsequent oocyte activation (25). It is of interest to note that, unlike in IVF, calcium oscillation in ICSI begins after a delay of approximately 30 minutes to several hours (26). DIFFERENT METHODS FOR ARTIFICIAL OOCYTE ACTIVATION Calcium transient is the key trigger of oocyte activation, including meiotic resumption during. Different procedures for AOA have been established and are commonly divided into three subtypes mechanical, electrical, and chemical stimuli that elicit one or several calcium transients (27, 28). During mechanical activation of oocytes, plasma membranes of the oocytes are broken using a microneedle to maintain a calcium influx, and after a short period, ICSI is performed (29). Another method for mechanical oocyte activation is the direct microinjection of calcium into an oocyte to increase intracellular calcium. When this procedure is applied to pig and human oocytes, and events normally occurring during normal are observed (30, 31). Although this latter method may effectively induce AOA, it is not common in clinical practice. Electrical stimulation is another type of AOA that induces calcium influx through the formation of pores in the plasma membrane. The efficiency of this procedure depends on pore size, ionic content of the medium, and cell type. Electrical oocyte activation has been successfully used on bovine and human oocytes (32 36). Electrical activation also has been shown to induce reactive oxygen species (37). Chemical compounds can also induce calcium increase and initiate oocyte activation. Chemical oocyte activation has been reported with the use of compounds such as ethanol (34, 38), calcium ionophore A (34, 39), ionomycin (40), puromycin (41), strontium chloride (34, 42), phorbol ester (43), and thimerosal (44). However, the use of these compounds for AOA has been mainly limited to animal models and case reports. These compounds promote the release of intracellular calcium stores, mobilize intracellular calcium by depletion of calcium stores, and facilitate the influx of extra cellular calcium ions. Some of these compounds may induce a single calcium rise in the oocyte while others may induce multiple calcium rises (28). However, human oocytes do not easily respond to universal activators of mammalian oocytes such as the aforementioned chemical components. To mimic the natural pattern of calcium rise after sperm penetration or to optimize the rate of human oocyte activation, these compounds are sometimes applied in combination (27). Artificial Oocyte Activation and ICSI Outcome Although AOA is used to improve rates in the clinical laboratory, the literature mainly focuses on case reports. There are few reports on AOA in large numbers of ICSI patients. Table 1 presents some of these studies in human cases that used AOA to improve rates and embryo quality. The improved quality of embryos in some reports may be related to optimal oocyte activation, as optimized calcium oscillations can effect embryo development (22, 23). Artificial Oocyte Activation and Clinical Setting A review of the literature reveals that successful pregnancies would be achieved by implementing AOA along with ICSI in cases with failed after ICSI (see Table 1). However, the safety of AOA in a clinical setting remains to be assessed. Examination of cytotoxic activity of these chemical components on gametes has shown that calcium ionophore Fertility and Sterility â 521

3 522 Nasr-Esfahani et al. Artificial oocyte activation and ICSI Vol. 94, No. 2, July 2010 TABLE 1 Literature studies on artificial oocyte activation for improved rate and embryo assessment in infertile patients. Study Type of study Type of AOA Criteria for AOA Type of oocyte Conclusion Tesarik et al. (55) Infertile couples CIA Unfertilized oocyte after ICSI Aged Fertilization rate improved after ICSI Battaglia et al. (56) Case report CIA Globozoospermia Aged Fertilization rate improved after ICSI Rybouchkin et al. (57) Case report Calcium Globozoospermia Pregnancy achieved chloride and CIA Tesarik et al. (58) Five infertile couples CIA Patients undergoing spermatid conception Fertilization rate increased in oocytes injected with whole spermatids and isolated Nakagawa et al. (59) 172 oocytes CIA and puromycin Unfertilized oocyte after ICSI Aged spermatid nuclei Two pronucleus, second polar body and cleavage observed Kim et al. (60) Case report CIA Globozoospermia Pregnancy achieved after frozen-thawed embryo transfer Eldar-Geva et al. (61) and Chi et al. (62) Case report CIA Previous failed Murase et al. (63) Case report CIA and puromycin Previous failed Heindryckx et al. (64) 17 patients Ionomycin Previous failed Lu et al. (47) (48) 113 discarded oocytes CIA and puromycin Unfertilized oocyte after ICSI Moaz et al. (65) 56 patients Ionomycin Previous failed Ahmady and Michael (66) Case report CIA Nonviable testicular sperm Check et al. (67) Case report CIA Globozoospermia and previous failed Nasr-Esfahani. Artificial oocyte activation and ICSI. Fertil Steril Aged High rate and pregnancy achieved High rate and pregnancy achieved High rates and pregnancy achieved in some patients Fertilization achieved Fertilization rate increased in patients with severe head abnormalities Pregnancy achieved No improvement in rate

4 Fertility and Sterility â 523 TABLE 1 Continued. Study Type of study Type of AOA Criteria for AOA Type of oocyte Conclusion Borges et al. (68) 204 patients CIA Surgical sperm retrieval for ICSI Fertilization rate, embryo quality, and pregnancy increased in azoospermic patients with epididymal but not testicular spermatozoa Tejera et al. (69) Case report CIA Globozoospermia Fertilization rate and embryo quality improved Heindryckx et al. (70) 30 patients CIA and injection of CaCl 2 Globozoospermia and oligoasthenotera Fertilization rate improved and pregnancy Nasr-Esfahani et al. (49) tozoospermia 87 patients Ionomycin Severe terato- and asthenospermia achieved Fertilization rate, higher embryo quality, and possibly pregnancy rate increased Yanagida et al. (42) 2 patients Electrical oocyte activation Previous failed 100% rate achieved Mansour et al. (36) 246 patients Electrical oocyte activation Severe oligoasthenospermia, nonobstructive azoospermia with totally immotile spermatozoa Fertilization rate improved in severe oligoasthenoteratospermia and nonobstructive azoospermia Yanagida et al. (33) Case report Strontium chloride Previous failed 100% rate and pregnancy achieved Kyono et al. (45) 9 patients Strontium chloride Previous failed High rate, embryo quality, and pregnancy achieved Dirican et al. (31) Case report Mechanical oocyte activation Two familial globozoospermia Pregnancy achieved with and without AOA Notes: Aged oocyte ¼ unfertilized oocyte 24 to 48 hours after in vitro (IVF) or intracytoplasmic sperm injection (ICSI); AOA ¼ artificial oocyte activation; CIA ¼ calcium ionophore A Nasr-Esfahani. Artificial oocyte activation and ICSI. Fertil Steril 2010.

5 A23187 in combination with puromycin and strontium chloride does not appear to be cytotoxic when used in an optimum concentration (27, 45). In addition, with AOA by calcium ionophore and puromycin, about 80% of unfertilized oocytes reveal a normal haploid set of chromosomes. This may suggest the MII oocytes that respond to the chemical component for AOA have an appropriate number of chromosomes (27), in contrast to reports of failed aged, unfertilized oocytes. Also, sex chromosomal analysis (by fluorescence in situ hybridization) has shown that embryos assessed after AOA have normal sex chromosome status (46 48). Furthermore, several studies thus far have revealed no physical or mental developmental disorders associated with babies born through this procedure, even 12 months after birth (45, 49). However, a major point that must be considered with these studies is a comparison of the type of patients addressed, along with their corresponding control groups. In our previous study, we reported that all patients may not benefit from AOA (49). Therefore, to identify which patients are candidates of AOA, additional diagnostic tests such as the mouse oocyte activation test (MOAT) may be useful to evaluate the activation potential of a semen sample before assisted AOA in the clinical setting (50). Because MOAT may be inconvenient in clinical settings, other tests such as the acrosome related test or gelation lysis test may be useful or at least informative for assessing acrosome integrity (which may related to oocyte activation capacity) (9, 49). Artificial Oocyte Activation and Globozoospermia A specific group of patients who often face failed are men with globozoospermia; a rare disorder characterized by round-headed, acrosomeless sperm cells (51). The lack of an acrosome is considered to be the cause of infertility in these patients (52, 53). The introduction of ICSI led to several successful pregnancies after ICSI with globozoospermic sperm in combination with AOA (see Table 1). Moreover, there are several reports of unsuccessful ICSI attempts in cases of globozoospermia in the absence of AOA (52). This suggests that, besides the inability to interact with the female gamete due to an abnormal acrosome, globozoospermic sperm may have additional defects that affect their capability. Some studies employing MOAT to analyze spermatozoa from globozoospermic men have indicated that they could not successfully activate oocytes (50). Currently, the presence of PLCz in sperm cells is under investigation, and preliminary data confirm that sperm from globozoospermic men contains lower amounts of PLCz as compared with normal sperm (54). In addition, other cases of failed may be explained by defects in the PLCz protein. CONCLUSION Artificial oocyte activation may be useful in selected patients when there is no or low potential and may be considered in male factor disorders such as globozoospermia, severe teratozoospermia, and nonobstructive azoospermia. A clinical test to evaluate the activation potential of semen samples would be useful, as would further verification of the biosafety of AOA. REFERENCES 1. Skakkebaek NE, Jørgensen N, Main KM, Rajpert-De Meyts E, Leffers H, Andersson AM, et al. Is human fecundity declining? Int J Andrologia 2006;29: Palermo G, Joris H, Devroey P, Van Steirteghem AC. Pregnancies after intracytoplasmic injection of single spermatozoon into an oocyte. Lancet 19924;340: Van Steirteghem AC, Nagy Z, Joris H, Liu J, Staessen C, Smitz J, et al. High and implantation rates after intracytoplasmic sperm injection. Hum Reprod 1993;8: Emery BR, Wilcox AL, Aoki VW, Peterson CM, Carrell DT. 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7 65. Moaz MN, Khattab S, Foutouh IA, Mohsen EA. Chemical activation of oocytes in different types of sperm abnormalities in cases of low or failed after ICSI: a prospective pilot study. Reprod Biomed Online 2006;13: Ahmady A, Michael E. Successful pregnancy and delivery following intracytoplasmic injection of frozen-thawed nonviable testicular sperm and oocyte activation with calcium ionophore. J Androl 2007;28: Check JH, Levito MC, Summers-Chase D, Marmar J, Barci H. A comparison of the efficacy of intracytoplasmic sperm injection (ICSI) using ejaculated sperm selected by high magnification versus ICSI with testicular sperm both followed by oocyte activation with calcium ionophore. Clin Exp Obstet Gynecol 2007;34: Borges E, Braga DPAF, Bonetti TC, Iaconelli A, Franco J. Artificial oocyte activation with calcium ionophore A23187 in intracytoplasmic sperm injection cycles using surgically retrieved spermatozoa. Fertil Steril 2008;90:S Tejera A, Molla M, Muriel L, Remohı J, Pellicer A, De Pablo JL. Successful pregnancy and childbirth after intracytoplasmic sperm injection with calcium ionophore oocyte activation in a globozoospermic patient. Fertil Steril 2008;90:1202.e1 e Heindryckx B, De Gheselle S, Gerris J, Dhont M, De Sutter P. Efficiency of assisted oocyte activation as a solution for failed intracytoplasmic sperm injection. Reprod Biomed Online 2008;17: Nasr-Esfahani et al. Artificial oocyte activation and ICSI Vol. 94, No. 2, July 2010

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