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Effects of Paternal Age on Human Embryo Development in in Vitrofertilization with Preimplantation Genetic Screening

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Effects of Paternal Age on Human Embryo Development in in Vitrofertilization with Preimplantation Genetic Screening ORIGINAL ARTICLE https://doi.org/10.5653/cerm.2019.46.1.22 pISSN 2233-8233 · eISSN 2233-8241 Clin Exp Reprod Med 2019;46(1):22-29 Effects of paternal age on human embryo development in in vitro fertilization with preimplantation genetic screening Min Kyoung Kim1, Jae Kyun Park1,2, Yunmi Jeon1, Su Hee Seok1, Eun Mi Chang1, Woo Sik Lee1 1Department of Obstetrics and Gynecology, Fertility Center of CHA Gangnam Medical Center, CHA University School of Medicine, Seoul; 2Department of Biomedical Science, CHA University, Seongnam, Korea Objective: As paternal age increases, the quality of sperm decreases due to increased DNA fragmentation and aneuploidy. Higher levels of structural chromosomal aberrations in the gametes ultimately decrease both the morphologic quality of embryos and the pregnancy rate. In this study, we investigated whether paternal age affected the euploidy rate. Methods: This study was performed using the medical records of patients who underwent in vitro fertilization (IVF) procedures with preim- plantation genetic screening (PGS) from January 2016 to August 2017 at a single center. Based on their morphological grade, embryos were categorized as good- or poor-quality blastocysts. The effects of paternal age were elucidated by adjusting for maternal age. Results: Among the 571 total blastocysts, 219 euploid blastocysts were analyzed by PGS (38.4%). When the study population was divided into four groups according to both maternal and paternal age, significant differences were only noted between groups that differed by maternal age (group 1 vs. 3, p=0.031; group 2 vs. 4, p=0.027). Further analysis revealed no significant differences in the euploidy rate among the groups according to the morphological grade of the embryos. Conclusion: Paternal age did not have a significant impact on euploidy rates when PGS was performed. An additional study with a larger sam- ple size is needed to clarify the effects of advanced paternal age on IVF outcomes. Keywords: Embryo quality; In vitro fertilization; Paternal age; Preimplantation genetic screening Introduction dergoing in vitro fertilization (IVF), the number of retrieved oocytes [1], fertilization rate [2], and implantation rate [3] are lower than in Couples delay childbearing due to higher education, increased par- younger patients. Paternal age is also increasing [4], but the effect of ticipation of women in the workforce, and improved contraception. paternal age on IVF has been studied much less, and the results are Assisted reproductive technology (ART) has also extended the repro- conflicting. ductive window. Many studies have shown that maternal age is a A systematic review of 10 studies on the association between pa- major factor that affects the success rate of ART. In older women un- ternal age and ART outcomes did not show clear correlations be- tween advanced paternal age and the rates of fertilization, implanta- Received: Nov 14, 2018 ∙ Revised: Jan 9, 2019 ∙ Accepted: Jan 25, 2019 tion, pregnancy, miscarriage, and live birth [5]. Another recent meta- Corresponding author: Woo Sik Lee Department of Obstetrics and Gynecology, Fertility Center of CHA Gangnam analysis investigated 12 studies on the influence of paternal age on Medical Center, CHA University School of Medicine, 569 Nonhyeon-ro, oocyte donation outcomes to exclude bias due to the factor of ma- Gangnam-gu, Seoul 06125, Korea Tel: +82-2-3468-3000 Fax: +82-2-3468-2609 E-mail: [email protected] ternal age [6]. Similarly, no statistically significant correlation be- tween advanced paternal age and clinical outcomes was found. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/) which permits In contrast, some studies reported negative effects of advanced pa- unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. ternal age on ART outcomes. For instance, 237 oocyte donation cy- 22 www.eCERM.org Copyright © 2019. THE KOREAN SOCIETY FOR REPRODUCTIVE MEDICINE MK Kim et al. Paternal age effect on human embryos cles were reviewed and the implantation rate significantly declined human chorionic gonadotropin (hCG) (Ovidrel, Merck) when there with increasing paternal age [7]. Each 5-year increase in paternal age were ≥2 follicles with a mean diameter ≥17 mm. Ultrasound-guid- was associated with 26% lower odds of live birth. An observational ed oocyte retrieval under conscious sedation was performed 34–36 study comparing sperm genomic decay in young and advanced pa- hours after the trigger. Luteal phase support was provided with pro- ternal age groups showed increased DNA fragmentation, chromatin gesterone vaginal suppositories (Utrogestan; Han Wha Pharma, decondensation, and sperm aneuploidy rates in older men [8]. IVF Seoul, Korea) starting on the day of ovum pick-up. The β-hCG level outcomes such as the decision to perform embryo transfer, the clini- was checked 10–12 days after embryo transfer. cal pregnancy rate, and the miscarriage rate were also negatively af- fected. Therefore, this study aimed to investigate the effect of pater- 3. Embryo culture, grading, and biopsy procedures nal age on euploidy in embryos and clinical outcomes after IVF and Intracytoplasmic sperm injection (ICSI) was used to fertilize all the preimplantation genetic screening (PGS). embryos from fresh cycles. Of the thawed embryo transfer (TET) cy- cles, ICSI was used in 57%, half-ICSI (ICSI and conventional IVF com- METHODS bined) in 15.9%, and conventional IVF in 27.1%, since for some pa- tients, clinicians decided to perform PGS after embryo cryopreserva- 1. Patients tion. For ICSI, the collected semen was liquefied for 30 minutes on a This was a retrospective study reviewing the medical records of in- 37°C hot plate, after which sperm motility was evaluated [10]. Semen fertile patients undergoing IVF procedures from January 2016 to Au- analysis was done, and semen samples with a normal sperm count gust 2017 at the Fertility Center of CHA Gangnam Medical Center. and motility were washed two times with 10% SPS including Ham’s Patients who responded normally to ovarian stimulation were re- F-10 media by centrifuge. Motile spermatozoa were collected using cruited. The normal responders were selected according to age, anti- the swim-up method. The general condition of each spermatozoon Müllerian hormone (AMH) levels, follicle-stimulating hormone (FSH) was thoroughly checked by first inspecting its general motility and levels, and number of aspirated oocytes. PGS at the blastocyst stage morphology (head, midpiece, and tail), and then its head shape was was offered to infertile patients of advanced age (≥35 years), and/or evaluated. A spermatozoon was considered to have normal mor- with ≥3 unexplained recurrent pregnancy losses and/or ≥3 recur- phology when its head length was 5–7 μm, its width was 2–3 μm, rent implantation failures. Patients who did not undergo PGS and and the acrosome distribution was more than 70% [11]. After select- those who underwent 3-day embryo transfer were excluded from ing normal sperm, ICSI was performed under microscopy with ×200 the study population. Study participants were grouped according to magnification. In total, ICSI was used in 73.7% of cycles, half-ICSI in age: women aged <35 years and men aged ≤38 years (group 1), 9.7%, and conventional IVF in 16.6%. Fertilization was confirmed women aged <35 years and men aged >38 years (group 2), women when the two-pronucleus stage was observed after 16–20 hours. aged ≥35 years and men aged ≤38 years (group 3), and women During the cleavage stage, embryos were cultured in cleavage medi- aged ≥35 years and men aged >38 years (group 4). The paternal um (Cook, Eight Mile Plains, Australia), and then transferred to blas- age cutoff of 38 years was defined according to the most equilibrat- tocyst medium (Cook) on day 3. ed distribution of cases in both age groups and on the basis of an- Embryos were cultured in incubators (HERAcell 240i; Thermo Fisher other study [9]. Scientific, Waltham, MA, USA) under 5% 2O and 6% CO2 at 37°C. Oil drop culture was done using a four-well dish (Nunc, Thermo Fisher 2. Clinical protocols Scientific). In 20-µL drops, a single round of embryo culture was car- Gonadotropin-releasing hormone (GnRH) antagonist and agonist ried out to facilitate the observation of embryonic development. protocols were mostly used in this study. The following medications Light paraffin oil (Ovoil; Vitrolife, Göteborg, Sweden) was dropped were used in these protocols: recombinant FSH (Gonal-F, Merck, onto the media to prevent it from drying or undergoing a rapid pH Darmstadt, Germany; Pergoveris, Merck), a GnRH antagonist (Cet- change. rotide, Merck), and a GnRH agonist (Lorelin; Dongkook Pharmaceuti- Morphological grading of the embryos after culture was done on cal, Seoul, Korea). Recombinant FSH doses were formulated accord- day 5 (Figure 1). Embryo quality on day 5 was assessed according to ing to the patient’s antral follicular count, AMH level, and previous re- the criteria of Gardner and Schoolcraft [12]. Good-quality embryos sponse to stimulation. on day 5 were defined as those with a blastocoel equal to or greater Transvaginal ultrasound was performed to monitor the follicular re- than half the volume of the embryo and a good inner cell mass and sponse to stimulation, and gonadotropin doses were adjusted ac- trophectoderm (TE). Based on the morphological grade, the embryos cordingly. Final oocyte maturation was triggered with recombinant were categorized as good-quality blastocysts (excellent, good, or av- www.eCERM.org 23 Clin Exp Reprod Med 2019;46(1):22-29 A C B D Figure 1. Examples of evaluations of human blastocyst morphology. (A) High-quality expanded blastocyst: type A ICM, type A TE. (B) High- quality hatched blastocyst: type A ICM, type A TE. (C) Low-quality hatching blastocyst: type C ICM, type C TE.
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