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Outcome of Assisted Reproductive Technology in Men with Treated and Untreated Varicocele: Systematic Male Fertility Review and Meta‑Analysis

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Outcome of Assisted Reproductive Technology in Men with Treated and Untreated Varicocele: Systematic Male Fertility Review and Meta‑Analysis Asian Journal of Andrology (2016) 18, 254–258 © 2016 AJA, SIMM & SJTU. All rights reserved 1008-682X www.asiaandro.com; www.ajandrology.com Open Access INVITED REVIEW Outcome of assisted reproductive technology in men with treated and untreated varicocele: systematic Male Fertility review and meta‑analysis Sandro C Esteves1, Matheus Roque2, Ashok Agarwal3 Varicocele affects approximately 35%–40% of men presenting for an infertility evaluation. There is fair evidence indicating that surgical repair of clinical varicocele improves semen parameters, decreases seminal oxidative stress and sperm DNA fragmentation, and increases the chances of natural conception. However, it is unclear whether performing varicocelectomy in men with clinical varicocele prior to assisted reproductive technology (ART) improve treatment outcomes. The objective of this study was to evaluate the role of varicocelectomy on ART pregnancy outcomes in nonazoospermic infertile men with clinical varicocele. An electronic search was performed to collect all evidence that fitted our eligibility criteria using the MEDLINE and EMBASE databases until April 2015. Four retrospective studies were included, all of which involved intracytoplasmic sperm injection (ICSI), and accounted for 870 cycles (438 subjected to ICSI with prior varicocelectomy, and 432 without prior varicocelectomy). There was a significant increase in the clinical pregnancy rates (OR = 1.59, 95% CI: 1.19–2.12, I 2 = 25%) and live birth rates (OR = 2.17, 95% CI: 1.55–3.06, I 2 = 0%) in the varicocelectomy group compared to the group subjected to ICSI without previous varicocelectomy. Our results indicate that performing varicocelectomy in patients with clinical varicocele prior to ICSI is associated with improved pregnancy outcomes. Asian Journal of Andrology (2016) 18, 254–258; doi: 10.4103/1008-682X.163269; published online: 23 October 2015 Keywords: assisted reproductive techniques; meta‑analysis; pregnancy outcome; systematic review; varicocele; varicocelectomy INTRODUCTION seminal oxidative stress and sperm DNA fragmentation, and increases Varicocele is defined as a dilatation of the pampiniform plexus seminal antioxidants.6,7,14,15 However, it is unclear whether performing veins. It is the most common cause of male infertility affecting about varicocelectomy in infertile males with clinical varicocele prior to ART 15%–20% of the general population and 35%–40% of men presenting improves treatment outcomes.16 for an infertility evaluation.1–3 Until now, the exact mechanisms that The objective of this study was to collect and summarize all ultimately lead to infertility are not fully understood despite the evidence that evaluated the benefit of varicocelectomy on ART fact that varicocele pathophysiology has been discussed for close to outcomes in nonazoospermic infertile men with clinical varicocele. five decades. The main theories postulate that venous reflux leading MATERIALS AND METHODS to elevated testicular temperature and oxidative stress are the key We followed the Preferred Reporting Items for Systematic Reviews elements.4,5 Equally debatable is the actual benefit of interventions and Meta-Analysis (PRISMA) statement to report the results of this although recent evidence indicates that treatment may improve the review.17 The study was exempted from Institutional Review Board chance of pregnancy in subfertile couples in whom varicocele is the approval as it did not involve any interventions in humans. only abnormal finding.6,7 Oxidative stress and elevated sperm DNA fragmentation have been Search strategy associated with varicocele-mediated infertility.4,6–11 Although sperm An exhaustive electronic search was performed using the MEDLINE with fragmented DNA can fertilize oocytes with apparently similar and EMBASE databases up to April 2015. There were no limits placed efficiency to sperm without DNA fragmentation, it has been found on the year of publication, but we restricted the search to articles that high DNA fragmentation negatively impacts embryo development published in English. We also searched among the references of the and may jeopardize pregnancy outcomes in assisted reproductive identified articles. The search combined relevant terms and descriptors technology (ART).12,13 There is fair evidence indicating that surgical related to varicocele, varicocelectomy, varicocele repair, IVF, ICSI, repair of clinical varicocele improves sperm parameters, decreases and ART. 1ANDROFERT, Center for Male Reproduction, Av. Dr. Heitor Penteado 1464, Campinas, SP 13075-460, Brazil; 2ORIGEN, Center for Reproductive Medicine, Rio de Janeiro, Av. Rodolfo de Amoedo 140, Rio de Janeiro, RJ 22620-330, Brazil; 3American Center for Reproductive Medicine, 10681 Carnegie Avenue, X-11, Cleveland, OH 44195, USA. Correspondence: Dr. SC Esteves ([email protected]) Received: 19 July 2015; Revised: 11 August 2015; Accepted: 18 August 2015 ART outcome in men with treated and untreated varicocele SC Esteves et al 255 Eligibility criteria and data extraction Table 1: Selection criteria of included studies (PICOS) This systematic review and meta-analysis included studies Included Excluded comparing ART outcomes of nonazoospermic patients with Population Couples undergoing IVF/ICSI and the Azoospermic/ clinical varicocele who underwent varicocelectomy prior to ART male partner diagnosed with clinical cryptozoospermic to those without prior varicocele repair. Clinical varicoceles were varicocele patients considered as those diagnosed based on the finding of varicose Intervention Varicocelectomy prior to IVF/ICSI Varicocele embolization veins in the spermatic cord either by visual inspection or palpation Comparison IVF/ICSI without previous varicocelectomy with or without the aid of the Valsalva maneuver during physical Outcomes Live birth rate examination with the patient standing.18 ART was defined as all Clinical pregnancy rate treatments or procedures that include the in vitro handling of Implantation rate both human oocytes and sperm or of embryos for the purpose of Miscarriage rate establishing a pregnancy. This included in vitro fertilization (IVF)/ Fertilization rate intracytoplasmic sperm injection (ICSI) and embryo transfer.19 Study type Any type For the purpose of this review, ART did not include assisted IVF: in vitro fertilization; ICSI: intracytoplasmic sperm injection insemination (artificial insemination) using sperm from either a woman’s partner or a donor. Table 2: Quality assessment of included trials The selection criteria are described in Table 1. In the first screening, Study Sequence Allocation Blinding Incomplete two independent authors (M.R. and S.C.E.) assessed all of the abstracts generation concealed outcome data retrieved from the search and then obtained the full manuscripts of Esteves et al.24 No Yes No No the citations that met the inclusion criteria. These authors evaluated Pasqualotto et al.25 No Yes No No the studies’ eligibility and quality, and they subsequently extracted the Shiraishi et al.2 No No No No data. Any discrepancies were solved by agreement and, if needed, they Gokce et al.26 No Yes No No reached a consensus with the third author (A.A.). Outcome measures model and applied the fixed-effects model. When the heterogeneity The pregnancy rates, both clinical pregnancy and live birth, were was >50% (I2 > 50%), we applied the random-effects model.21 We used the primary outcomes of interest. Secondary outcomes included the Review Manager 5 software (Version 5.3. Copenhagen: The Nordic fertilization rate, implantation rate, and miscarriage rate. Clinical Cochrane Centre, The Cochrane Collaboration, 2014) to conduct pregnancy was defined as a pregnancy observed sonographically by the the meta-analysis. It was not possible to perform a meta-analysis for visualization of a fetal heartbeat by 7 weeks of gestation. The clinical implantation, miscarriage, and fertilization rates due the nature of the pregnancy rate was the number of clinical pregnancies expressed studies evaluating these outcomes. per 100 embryo transfers. The live birth rate was defined as the ratio between the number of deliveries resulting in at least one live birth RESULTS and the number of embryo transfers. Miscarriage was defined as a Our electronic search retrieved 114 articles. After screening the nonviable clinical pregnancy on ultrasound follow-up until gestational titles and abstracts, we determined that six articles were eligible for week 20. The implantation rate was defined as the number of gestational inclusion. Among these, two articles were excluded. One of them 22 sacs observed sonographically divided by the number of transferred was a review article, and the other study did not fulfill the inclusion 23 embryos. The fertilization rate was defined by the number of two criteria as the primary comparison was between patients submitted pronuclei zygotes divided by the number of metaphase II oocytes to varicocelectomy and observation. Although the authors of this subjected to sperm injections. aforementioned study evaluated ART outcomes in patients who did not achieve natural pregnancy after varicocele repair, they have included Risk of bias assessment intrauterine insemination as an ART treatment modality. As stated in We followed the guidance recommended by the Cochrane the eligibility criteria, the objective of our study was to compare only Collaboration to assess the risk of bias from the included studies.20 patients submitted to ART as per the ICMART definition. The complete We evaluated
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