Skip to main content
NCBI home page
American Journal of Men's Health logoLink to American Journal of Men's Health
. 2025 Apr 28;19(2):15579883251334561. doi: 10.1177/15579883251334561

Influence of Varicocelectomy on Assisted Reproductive Technology Outcomes of Infertile Patients with Varicocele: A Systematic Review and Meta-Analysis

Wending Teng 1, Jianfeng Xiao 2, Qian Xu 3, Penghao Li 3,✉
PMCID: PMC12038214  PMID: 40293106

Abstract

Varicocele can lead to impaired semen parameters and induce infertility. Varicocelectomy is considered the gold standard for varicocele treatment. However, its impact on improving assisted reproductive technologies (ARTs) outcomes remains contentious. This study seeks to compare reproductive outcomes between infertile men who underwent varicocelectomy and those who did not prior to ARTs. In addition, it evaluates the influence of types of fertilization, couples’ ages, and treatment years on clinical pregnancy rates. A comprehensive search was conducted through February 2023 across eight electronic databases using combinations of relevant keywords. Observational and randomized controlled trials (RCTs) were included. Fourteen eligible studies (n = 1,705) were included: 12 retrospective studies (n = 1,467) and 2 prospective studies (n = 238). Pooled results indicated that infertile men who received varicocelectomy had a significantly higher clinical pregnancy rate compared to the control group (OR: 1.38, 95% CI [1.05, 1.83]; I2 = 36%, p = .02). The live birth rate was also significantly higher in the treatment group (OR: 2.18, [1.58, 3.01]; p < .00001; I2 = 0%). However, miscarriage rates did not significantly differ (OR: 1.07; [0.57, 1.98]; I2 = 0%, p = .84). Varicocelectomy significantly improved sperm concentration and normal morphology rate, but did not result in a significant enhancement in sperm motility. Men who underwent varicocelectomy between 2012 and 2019 and subsequently received intracytoplasmic sperm injection exhibited improved outcomes, particularly when their female partners were under 30 years of age. Larger, high-quality RCTs are needed to clarify benefits or avoid unnecessary treatments.

Keywords: varicocelectomy, ARTs, pregnancy rate, live birth rate, ICSI

Introduction

Varicocele, characterized by the abnormal dilation of the pampiniform plexus veins in the scrotum, is a prevalent condition associated with male infertility (Jellad et al., 2021; Santana et al., 2019; Y. Zhang et al., 2022). Early research indicated that men with varicocele had higher scrotal temperatures compared to those without varicocele (Garolla et al., 2015; Goldstein & Eid, 1989). It was previously hypothesized that the testicular hyperthermia caused by varicocele might be associated with impaired sperm parameters (Garolla et al., 2015; Goldstein & Eid, 1989). Past studies have supported that infertile men with varicocele have higher levels of reactive oxygen species (ROS), nitric oxide, and lipid peroxidation products (Cho et al., 2016; Mostafa et al., 2009). In addition, elevated ROS levels are related to impaired sperm concentration, motility, morphology, and sperm DNA fragmentation (SDF) (Agarwal et al., 2014).

Varicocelectomy has been considered the gold standard for varicocele therapy and offers a better prognosis when compared with other treatments (Baazeem et al., 2011; Birowo, Tendi et al., 2020; Johnson & Sandlow, 2017). Numerous studies and systematic reviews have demonstrated the benefits of varicocelectomy in reducing SDF and enhancing semen parameters such as sperm concentration, motility, and morphology (Al-Mohammady et al., 2019; Birowo, Rahendra Wijaya et al., 2020; Inci et al., 2009; Nakonechnyi et al., 2022; Soetandar et al., 2022). Varicocelectomy can also enhance the chances of spontaneous pregnancy (Peng et al., 2015). However, the development of advanced assisted reproductive technologies (ARTs) has enabled many infertile couples to achieve pregnancy (Inhorn & Patrizio, 2015). ARTs can also serve as an alternative to varicocelectomy for managing clinical varicocele with abnormal semen parameters (Sonmez & Haliloglu, 2018). Some reports suggested that despite improved semen quality post-surgery, a significant number of patients still require ARTs to achieve pregnancy (J. R. Kohn et al., 2020; T. P. Kohn et al., 2017). The reason might be that varicocelectomy typically does not fully restore normal sperm parameters in men. The procedure often improves semen parameters to a degree that allows men to attempt intrauterine insemination (IUI), whereas previously their sperm counts would have only qualified them for in vitro fertilization (IVF) or intracytoplasmic sperm injection (ICSI) (Dubin et al., 2018; Wang et al., 2019). Although the majority of patients opt for laparoscopic and microsurgical varicocelectomy due to its minimally invasive nature compared to open surgery, the risk of complications such as hematoma, wound infection, postoperative pain, and recurrence persists (Ameli et al., 2019). Therefore, it is critical to understand whether varicocelectomy can significantly improve ART outcomes, or whether it merely serves as an adjunct to these techniques.

Moreover, clinicians remain cautious regarding the potential impact of clinical parameters of varicocelectomy on reproductive outcomes until further evidence becomes available (Al-Mohammady et al., 2019; J. R. Kohn et al., 2020). Previous studies offered additional insights into optimizing outcomes through patient selection and individualized treatment approaches (Jensen et al., 2017; J. R. Kohn et al., 2020). Personalized treatment plans should consider the patient’s specific condition, including fertilization type and the age of the patient (Carson & Kallen, 2021; J. R. Kohn et al., 2020). Given the varying patient conditions, the substantial costs, and the potential risks associated with varicocelectomy, this understanding is critical for identifying which type of patients are most likely to benefit from varicocele treatment, particularly those who have already planned to seek the assistance of ART (Al-Mohammady et al., 2019; Inci et al., 2009; Pasqualotto et al., 2012).

Therefore, this meta-analysis aims to systematically evaluate the existing evidence on the impact of varicocelectomy on ART outcomes. By aggregating data from multiple studies, this analysis seeks to identify which patient populations are most likely to benefit from surgical intervention prior to ARTs. This comprehensive review will contribute to more informed clinical decision-making and optimize treatment strategies for couples facing infertility challenges.

Methods

Search Strategy

A comprehensive search was performed in the English databases of PubMed, Ovid, Medline, Embase, and Cochrane Library, as well as Chinese databases of China National Knowledge Infrastructure, and Cqvip and Wanfang. The date restriction was set up to February 2023. Medical Subject Headings terms included: “Assisted Reproductive Technique” and “Varicocelectomy.” The search strategy is detailed in Table 1.

Table 1.

Search Strategy

No. Medical subject headings terms
1. ART/assisted reproductive technique/reproductive technique, assisted/technique, assisted reproductive/techniques, assisted reproductive/assisted reproductive technics/assisted reproductive technic/reproductive technic, assisted/reproductive technics, assisted/technic, assisted reproductive/technics, assisted reproductive/assisted reproductive techniques/reproductive technology, assisted/assisted reproductive technologies/assisted reproductive technology/reproductive technologies, assisted/technologies, assisted reproductive/technology, assisted reproductive
2 ET/embryo transfers/transfer, embryo/transfers, embryo/blastocyst transfer/tubal embryo transfer/tubal embryo stage transfer
3 ICSI/injection, intracytoplasmic sperm/injections, intracytoplasmic sperm/intracytoplasmic sperm injection/sperm injection, intracytoplasmic/intracytoplasmic sperm injections/injections, sperm, intracytoplasmic
4 IVF/in vitro fertilization/in vitro fertilizations/test-tube fertilization/fertilization, test-tube/fertilizations, test-tube/test tube fertilization/test-tube fertilizations/fertilizations in vitro/test-tube babies/babies, test-tube/baby, test-tube/test tube babies/test-tube baby
5 Intrauterine insemination/IUI/eutelegenesis/eutelegeneses/artificial insemination/artificial inseminations/inseminations, artificial
6 1 OR 2 OR 3 OR 4 OR 5
7 Varicocele/varicocelectomy/varicocele treatment/varicocele repair
8 6 and 7
Open in a new tab

Inclusion and Exclusion Criteria

Inclusion criteria: (a) the case group was infertile male patients treated with varicocelectomy; (b) the control group was infertile male patients without treatment; (c) the original available data were provided in articles.

Exclusion criteria: (a) reviews, case reports, commentaries, and letters to the Editor article types; (b) duplicated publications; (c) studies without a control group; (d) subjects without ART utility data; (e) subjects who conceived naturally.

Data Extraction and Quality Assessment

Two researchers independently and carefully extracted available information from each eligible study: (a) author’s last name, (b) year of publication, (c) country, (d) study design, (e) sample size of cases and controls, (f) surgical approaches, (g) male age, (h) female age, (i) control, (j) fertilization type, (k) disease, (l) grade of varicocele, (m) semen characteristics, and (n) outcome measures. Quality assessment was independently conducted by two investigators, with discrepancies resolved by a third investigator. The risk of bias in randomized controlled trials (RCTs) was appraised using Cochrane’s tool. The quality of cohort studies was evaluated using the Newcastle-Ottawa Scale, with scores ranging from 0 to 9 points, encompassing three domains: selection, comparability, and exposure.

Statistical Analysis

The extracted data were analyzed with Review Manager 5.3 software (Cochrane Collaboration, Oxford, U.K.). The Mantel-Haenszel method and random-effects models were used for meta-analysis. The effect sizes were expressed as odds ratios (ORs) and calculated using their 95% confidence intervals (CIs). Summary ORs and 95% CIs were assessed graphically with forest plots. Heterogeneity was quantified by the I2 value. Sensitivity analysis was used to assess whether there was any study affecting the stability of the results. A p-value < .05 was considered statistically significant.

Results

Database Search and Characteristics of Included Studies

As shown in Figure 1, we first searched 838 publications (154 from CNKI, 49 from Cqvip, 142 from Wanfang, 154 from PubMed, 22 from Ovid, 141 from Medline, 140 from Embase, and 36 from Cochrane Library), of which 298 were removed as duplicates. After record screening, 519 studies were excluded for not fulfilling the experimental criteria. Among these, seven articles were excluded after reading the title and abstract and confirming that they did not meet the inclusion conditions were matched. We then downloaded 14 selected articles (13 English and 1 Chinese) and analyzed them carefully. The main characteristics of the included studies are shown in Table 2. The publication dates of the eligible studies ranged up to 2023. The number of patients ranged from 39 to 306. Two studies were prospective studies (Al-Mohammady et al., 2019; Ketabchi et al., 2018), and twelve studies were retrospective studies (Baazeem et al., 2009; Boman et al., 2008; Daitch et al., 2001; Esteves et al., 2010; Gokce et al., 2013; Haydardedeoglu et al., 2010; Huan et al., 2019; Inci et al., 2009; Marmar et al., 1992; O’Brien et al., 2004; Pasqualotto et al., 2012; Zini et al., 2008). RCTs were reported in one of the two prospective studies. The quality assessments for the RCTs and cohort studies were summarized in Tables 3 and 4.

Figure 1.

Figure 1.

Open in a new tab

Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) Flowcharts

Table 2.

Main Characteristics of the Included Studies

Author Year Country Study design Recruited patients number Surgical approach(es) Male age (years) Female age (years) Control Fertilization Disease Grade of varicocele Semen characteristics Outcome measures
Case Control Case Control Case Control
Al-Mohammady 2018 Egypt A prospective comparative study 50 50 Varicocele repair — — 27.680 ± 3.846 28.780 ± 4.122 Untreated ICSI Non-azoospermic infertile men with a history of varicocele All grades Non-azoospermic Biochemical and clinical pregnancy rate
Baazeem 2008 Canada Retrospective study 72 54 Microsurgical varicocelectomy 34.9 ± 5.5 36.2 ± 5.5 33.1 ± 4.0 33.0 ± 4.5 Untreated IUI and ICSI Oligospermic men with varicocele All grades Consecutive oligospermic Pregnancy rates
Boman 2008 Canada Retrospective study 69 49 Microsurgical varicocelectomies 35.9 ± 4.5 38.3 ± 5.8 34.0 ± 2.9 33.9 ± 5.2 Untreated IUI and ICSI 1 year or more of infertility, a clinically palpable varicocele All grades Asthenospermia Pregnancy rates
Daitch 2001 America A Retrospective comparative study 34 24 Inguinal Ivanissevich or subinguinal microsurgical approach — — — — Untreated IUI Varicocele All grades Oligospermia asthenospermia, teratospermia (any combination of) Clinical pregnancy and live birth rate
Esteves 2010 Brazil Retrospective study 80 162 Subinguinal microsurgical varicocelectomy 35.8 ± 5.4 35.4 ± 6.3 32.6 ± 4.4 32.2 ± 4.3 Untreated ICSI Clinical unilateral or bilateral varicocele All grades Oligospermia asthenospermia, teratospermia (any combination of) Clinical pregnancy, miscarriage and live birth rate
Gokce 2013 Turkey Retrospective study 168 138 Subinguinal microsurgical varicocelectomy 34.8 ± 4.3 34.4 ± 4.1 29.7 ± 3.9 30.1 ± 4.0 Untreated ICSI Clinical varicocele All grades Oligospermia asthenospermia, teratospermia (any combination of) Clinical pregnancy and miscarriage rate
Haydardedeoglu 2009 Turkey Retrospective study 31 65 Macrosurgical varicocelectomy operation 35.0 ± 6.40 35.20 ± 6.09 28.74 ± 5.19 29.43 ± 3.9 Untreated ICSI with TESE Nonobstructive azoospermia Only grade III Nonobstructive azoospermia Implantation, clinical pregnancy and live birth rate
Inci 2009 Turkey Retrospective study 35 9 Testicular artery and lymphatic sparing inguinal or subinguinal microsurgical varicocelectomy 35.8 ± 5.6 34.7 ± 7.3 31.7 ± 4.9 30.3 ± 6.9 Untreated ICSI with TESE Nonobstructive Azoospermia All grades Nonobstructive azoospermia Clinical pregnancy, miscarriage and live birth rate
Ketabchi 2018 Iran Randomized clinical trial 67 71 Sub inguinal
microscopical varicocelectomy		 24 ± 3.7 26 ± 2.8 — — Untreated IUI, IVF and ICSI Infertile clinical varicocele All grades Semen parameter abnormality Pregnancy rates
Li 2019 China Retrospective study 29 31 Palomo varicocelectomy with preserving artery 30.25 ± 6.91 31.37 ± 5.59 28.23 ± 4.77 27.82 ± 5.13 Untreated IUI Infertile clinical varicocele All grades — Clinical pregnancy rate
Marmar 1992 America Retrospective Trial 14 34 Varicocelectomies 34.6 ± 4.1 32.4 ± 4.3 Untreated IUI Varicoceles All grades — Pregnancy rate
O’Brien 2004 Canada Retrospective study 14 25 Microsurgical varicocelectomy 39.06 ± 0.5 39.3 ± 60.5 37.4 6 ± 0.3 38.56 ± 0.3 Untreated IUI, IVF/ ICSI ≥1 year or more of infertility, a clinically palpable varicocele All grades Abnormal semen parameters Clinical pregnancy rate
Pasqualotto 2012 Brazil Retrospective study 79 169 Varicocelectomy 37.8 6 ± 0.47 36.16 ± 0.55 33.8 6 ± 0.38 33.06 ± 0.46 Untreated ICSI Varicocele grade Ⅲ grade Ⅲ Poor semen parameters Implantation, clinical pregnancy and miscarriage rate
Zini 2007 Canada Retrospective study 95 77 Microsurgical varicocelectomy 35.6 ± 5.6 35.9 ± 5.3 34.2 ± 4.4 33.5 ± 4.9 Untreated IUI and ICSI ≥1 year of infertility, a clinically palpable varicocele All grades Abnormal semen parameters Clinical pregnancy rate
Open in a new tab

Note. ICSI = intracytoplasmic sperm injection; IUI = intrauterine insemination; TESE = testicular epididymal sperm extraction; IVF = in vitro fertilization.

Table 3.

Risk of Bias Assessment of the Randomized Controlled Trials for Meta-Analysis Using the Cochrane Tool

Study Selection bias Performance bias Detection bias Attrition bias Reporting bias
Random sequence generation Allocation concealment Blinding of participants and personnel Blinding of outcome Incomplete outcome data Selective reporting
Ketabchi (2018) Low Low Unclear Unclear Low Low
Open in a new tab

Table 4.

Quality Assessment of the Cohort Studies for the Meta-Analysis Using the Newcastle-Ottawa Scale

Study Selection Comparability Outcome Score
Representativeness of the exposed cohort Selection of the nonexposed cohort Ascertainment of exposure Demonstration that outcome of interest was not present at start of study Comparability of cohorts on the basis of the design or analysis Assessment of outcome Was follow-up long enough for outcomes to occur Adequacy of follow-up of cohorts
Al-Mohammady (2018) 1 1 1 1 0 1 0 1 6
Baazeem (2008) 1 1 1 0 2 1 1 1 8
Boman (2008) 1 1 1 0 2 1 1 1 8
Daitch (2001) 1 1 1 0 0 1 0 0 4
Esteves (2010) 1 1 1 0 2 1 0 0 6
Gokce (2013) 1 1 1 0 2 1 0 0 6
Haydardedeoglu (2009) 1 1 1 0 2 1 0 0 6
Inci (2009) 1 1 1 0 2 1 0 0 6
Li (2019) 1 1 1 0 2 1 0 0 6
Marmar (1992) 1 1 1 0 1 1 0 0 5
O’Brien (2013) 1 1 1 0 2 1 1 1 8
Pasqualotto (2012) 1 1 1 0 2 1 0 1 7
Zini (2007) 1 1 1 0 2 1 1 1 8
Open in a new tab

Effects of Varicocelectomy on the Reproductive Outcomes of Infertile Patients

The clinical pregnancy rate outcomes were based on the data derived from 14 studies (872 cases and 833 controls). In retrospective studies, there was no significant difference between the two groups (OR: 1.32, 95% CI [0.95, 1.83]; p = .10; heterogeneity; I2 = 42%). In prospective studies, the clinical pregnancy rate was significantly higher in the case group than in the control group (OR: 1.79, [1.05, 3.06]; p = .03; heterogeneity; I2 = 0%). Overall, the clinical pregnancy rate was significantly higher in the case group than in the control group in a total of 14 studies (OR: 1.38, [1.05, 1.83]; p = .02; heterogeneity; I2 = 36%; Figure 2A).

Figure 2.

Figure 2.

Open in a new tab

Meta-Analyses of the Effect of Varicocelectomy on the Reproductive Outcomes of Infertile Patients with Varicocele. (A) Clinical Pregnancy Rate. (B) Live Birth Rate. (C) Miscarriage

The live birth rate outcomes were based on the data derived from five studies (348 cases and 398 controls). The live birth rate was significantly higher in the case group than in the control group (OR: 2.18, 95% CI [1.58, 3.01]; p < .00001; heterogeneity; I2 = 0%; Figure 2B).

However, the miscarriage rate outcomes were based on the data derived from three studies (284 cases and 250 controls). No difference was found in the miscarriage rate between the case and control groups (OR: 1.07, 95% CI [0.57, 1.98]; p = .84; heterogeneity; I2 = 0%; Figure 2C).

The Effects of Varicocelectomy on Sperm Parameters

The sperm concentration was significantly higher in the case group than in the control group (OR: 1.86, 95% CI [1.37, 2.35]; p < .00001; heterogeneity; I2 = 100%). The motility rate of sperm was significantly lower in the case group than in the control group (OR: −3.10, [−3.43, −2.76]; p < .00001; heterogeneity; I2 = 100%). The morphology rate of sperm was significantly higher in the case group than in the control group (OR: 0.32, [0.22, 0.43]; p < .00001; heterogeneity; I2 = 99%, Figure 3).

Figure 3.

Figure 3.

Open in a new tab

Forrest Plot for the Effect of Varicocelectomy on the Sperm Parameters. (A) sperm concentration. (B) motility rate of sperm. (C) morphology rate of sperm.

The Clinical Pregnancy Rate in Studies with Different Fertilization Types

No significant difference was found in the clinical pregnancy rate between the case and control groups when the fertilization type was IUI (OR: 1.65, 95% CI [0.65, 4.20]; p = .29; heterogeneity; I2 = 51%). When the infertile patients were treated with ICSI, the clinical pregnancy rate was significantly higher in the case group than in the control group (OR: 1.43, [1.01, 2.02]; p = .04; heterogeneity; I2 = 29%). No significant difference was found in the clinical pregnancy rate between the case and control groups when the fertilization type was ICSI with testicular epididymal sperm extraction (TESE) (OR: 2.20, [0.96, 5.04]; p = .06; heterogeneity; I2 = 0%; Figure 4).

Figure 4.

Figure 4.

Open in a new tab

Forrest Plot for the Effect of Varicocelectomy on the Clinical Pregnancy Rate in Studies with Different Fertilization Types

The Clinical Pregnancy Rate in Studies with Different Male and Female Ages

Regardless of whether the mean age of infertile male patients was less than 30, between 30 and 35, or more than 35 years, no significant difference in the clinical pregnancy rate was observed between the case and control groups (Not applicable, p = .13; OR: 1.34, 95% CI [0.63, 2.86]; p = .44; heterogeneity, I2 = 66%; OR: 1.22, [0.83, 1.79]; p = .31; heterogeneity, I2 = 29%; Figure 5A).

Figure 5.

Figure 5.

Open in a new tab

Forrest Plot for the Effect of Varicocelectomy on the Clinical Pregnancy Rate in Studies with Different Peer Review Mean Ages. (A) Male. (B) Female

When the mean age of female partners of infertile patients was less than 30 years, the clinical pregnancy rate was significantly higher in the case group than in the control group (OR: 2.03, 95% CI [1.43, 2.89]; p < .0001; heterogeneity, I2 = 0%). However, for female partners aged 30 to 35 years, there was no significant difference in the clinical pregnancy rate between the case and control groups (OR: 1.01, [0.69, 1.48]; p = .95; heterogeneity, I2 = 32%). Similarly, no significant difference was observed when the female partners were older than 35 years (Not applicable, p = .64; Figure 5B).

The Clinical Pregnancy Rate in Studies with Different Treatment Years

In infertile patients who underwent treatment from 1992 to 2001 and 2002 to 2011, no statistically significant difference in clinical pregnancy rates was observed between the case and control groups (OR: 2.36, 95% CI [0.81, 6.86]; p = .11; heterogeneity; I2 = 0%. OR: 1.11, [0.68, 1.82]; p = .67; heterogeneity; I2 = 51%). However, when patients underwent varicocelectomy between 2012 and 2019, the clinical pregnancy rate was significantly higher in the case group compared to the control group (OR: 1.59, [1.18, 2.14]; p = .002; heterogeneity; I2 = 5%; Figure 6).

Figure 6.

Figure 6.

Open in a new tab

Forrest Plot for the Effect of Varicocelectomy on the Clinical Pregnancy Rate in Studies with Different Treatment Years

Sensitivity Analysis

The results of the sensitivity analysis are shown in Figure 7. It was suggested that the elimination of no single study had a remarkable effect on the merged results, and the conclusions of this study were statistically reliable.

Figure 7.

Figure 7.

Open in a new tab

Sensitivity Analysis for the Effect of Varicocelectomy on Clinical Pregnancy Rate of Infertile Patients with Varicocele Using Random Effect Model (Odds Ratio)

Discussion

Clinically, the results of this meta-analysis suggest that varicocelectomy can be considered a viable treatment option for improving clinical pregnancy and live rates in infertile patients with varicocele, but it fails to reduce the miscarriage rates. The overall I2 value is less than 50%, which indicates that the conclusion is reliable. These findings align with previous investigations that have reported improved reproductive outcomes following varicocelectomy (Baazeem et al., 2011; Kirby et al., 2016; Sonmez & Haliloglu, 2018). Compared to the control group, the case group exhibits a significant increase in sperm concentration and normal morphology rates; however, a similar improvement is not observed in sperm motility. The overall I2 value exceeds 50%, likely due to the inclusion of studies published between 1992 and 2019, during which the criteria for sperm selection underwent significant changes (Vasconcelos et al., 2022; X. Z. Zhang et al., 2011). In addition, various laboratories employ different selection criteria. Seventy percent of studies published in two leading reproduction journals (Human Reproduction and Fertility & Sterility) between 2011 and 2020 cited WHO5, while 10% referenced WHO4, 7% cited both WHO4 and WHO5, 1% cited WHO3, and 12% did not reference WHO at all (Vasconcelos et al., 2022).

Subgroup analysis of fertilization types reveals that a significantly increased pregnancy rate is observed exclusively in patients undergoing ICSI, with no such increase noted in patients undergoing IUI and ICSI-TESE. These results are in agreement with Esteves et al. and Gokce et al. (Esteves et al., 2010; Gokce et al., 2013). Our findings show that varicocelectomy improves normal sperm morphology rates. Furthermore, prior research has shown that morphology significantly influences blastocyst formation rates and the development of high-quality blastocysts by Day 6 in ICSI treatment (Jiang et al., 2024). Although sperm motility is significantly associated with IUI outcomes, the lack of improvement in sperm motility after varicocelectomy results in no significant difference in pregnancy rates following IUI (Taniguchi et al., 2024). Although sperm concentration significantly increased, the total progressive motile sperm count does not significantly influence the success rate of IUI (Lin et al., 2022; Lin et al., 2021). O’Brien et al. demonstrated the utility rate of IVF/ICSI collectively, rather than the utility rate of IVF alone; there is no precise data available for the IVF population (O’Brien et al., 2004). Only Ketabchi et al. provided pregnancy data comparing the IVF group with the control group (Ketabchi et al., 2018). Consequently, a subgroup analysis for IVF was not performed. TESE is frequently necessary due to a low sperm count in the ejaculate for some individuals and due to azoospermia recurrence following the recovery of spermatogenesis in others (F. Zhang et al., 2024). A high frequency of karyotype abnormalities or Y-chromosome deletions has been detected in azoospermic men (Cioppi et al., 2021; Lahoz Alonso et al., 2023). Men with nonobstructive azoospermia (NOA) have mutations in genes critical for spermatogenesis (AP1S2, AP1G2, and APOE) (Cheung et al., 2024). Individuals with NOA-related infertility possess mutations in genes related to spermatogenesis /spermiogenesis (ADAM29, SPATA31E1, MAK, POLG, IFT43, and ATG9B) and early embryonic development (MBD5, CCAR1, PMEPA1, POLK, REC8, REPIN1, MAPRE3, and ARL4C) (Cheung et al., 2024). Varicocelectomy does not alter genetic infertility, which might explain why ICSI-TESE men do not experience improved clinical pregnancy rates.

In recent years, there has been a global trend of women delaying childbearing, resulting in a rise in the average paternal and maternal age (Bhasin et al., 2019). Advanced paternal age is associated with a higher risk of spontaneous miscarriage (du Fossé et al., 2020). Maternal age is a crucial factor influencing oocyte quality, with advanced maternal age associated with higher risks of chromosome segregation errors and aneuploidy in oocytes (Charalambous et al., 2023; Mikwar et al., 2020). Given the potential influence of patient age at the time of varicocelectomy on ART outcomes, a detailed subgroup analysis was performed. The results indicate that male age does not significantly alter pregnancy outcomes. In contrast, female age has a significant impact on the clinical pregnancy rate. Notably, the results show that male patients significantly benefit from the varicocelectomy when the mean age of female partners is less than or equal to 30 years old. This observation is consistent with the established notion that the effect of paternal age is less pronounced than the impact of advanced maternal age on reproductive outcomes (du Fossé et al., 2020). Considering the high quality of oocytes from young women, the reproductive benefits are preserved due to the enhanced sperm quality following varicocelectomy. However, the adverse effects of advanced maternal age may counteract any positive impact of varicocelectomy. Therefore, it is plausible to observe no significant difference in clinical pregnancy rates between the two groups when the mean age of female patients exceeds 30 years in our study. In addition, previous research has shown that the recovery period following varicocelectomy varies (Al-Mohammady et al., 2019; Haydardedeoglu et al., 2010; Pasqualotto et al., 2003). Pasqualotto et al. observed that the duration from surgery to pregnancy in the varicocelectomy group was significantly extended, measuring 6.0 ± 0.49 months, compared to 2.7 ± 0.36 months in the untreated group (Pasqualotto et al., 2003). Al-Mohammady et al. demonstrated that the minimum time from varicocelectomy to ICSI was 12 months (Al-Mohammady et al., 2019). Haydardedeoglu et al. found a significant time interval between varicocele repair and TESE (Haydardedeoglu et al., 2010). In the pregnant varicocele repair group, this period was up to 42 months, while in the nonpregnant group, it reached 80 months (Haydardedeoglu et al., 2010). This delay in childbearing poses additional challenges for couples facing infertility, particularly when the male partner undergoes varicocelectomy. The recovery period after varicocelectomy can take approximately 6 to 80 months, which can be a significant duration for couples with advanced maternal age (J. R. Kohn et al., 2020; H. Li et al., 2022). The combined effect of advanced maternal age and the time required for postoperative recovery can result in heightened challenges for achieving successful pregnancies through ARTs (Gourinat et al., 2023; Ribeiro & Sousa, 2023). Given the critical importance of each reproductive cycle for patients of advanced maternal age, our findings indicate that correcting the varicocele prior to ARTs is unnecessary for female partners over the age of 30.

Due to the incomplete surgical information provided in the articles, a subgroup analysis was conducted based on treatment years rather than surgical methods, leading to the following conclusions. Patients treated between 2012 and 2019 experienced significant benefits, while those treated in the periods 1992 to 2001 and 2002 to 2011 did not enjoy the same advantages. Between 1992 and 2019, technological advancements drove changes in varicocelectomy techniques. For instance, minimally invasive procedures such as embolization and sclerotherapy reduced recovery times and complications, while open surgeries, including inguinal and high ligation techniques, were tailored to different patient needs (Binhazzaa et al., 2016; Motta et al., 2019; Nabi et al., 2004). The Palomo procedure, using a retroperitoneal approach, provided improved visibility and operational space (Chung et al., 2023; Sepúlveda et al., 2018). The introduction of microsurgical techniques greatly enhanced surgical precision, reducing recurrence rates, and laparoscopic methods further streamlined the process, shortening hospital stays and speeding up recovery (Motta et al., 2019; Sepúlveda et al., 2018). These advancements not only improved treatment outcomes but also enhanced the overall patient recovery experience. The time-based analysis effectively highlights the impact of evolving surgical techniques on treatment outcomes.

Our study has several limitations that should be addressed in future research. The heterogeneity in our analysis might be attributed to differences in study designs and varicocele grading. Among the fourteen included articles, only one was an RCT. Therefore, larger, well-designed RCTs are needed to confirm our findings. Previous studies have suggested that higher-grade varicoceles may have a more pronounced negative impact on fertility, and thus, the benefits of surgical intervention might vary accordingly (X. Li et al., 2020). The data based on the grade of varicocele in recruited articles were limited; thus, the potential impact of surgical intervention on ARTs in patients with various grades of varicocele has not been comprehensively analyzed. More detailed subgroup analyses associated with grades of varicocele are required. Future research should continue to elucidate the mechanisms through which varicocelectomy improves reproductive outcomes.

Conclusion

In summary, this meta-analysis indicates that varicocelectomy significantly improves clinical pregnancy and live birth rates in infertile patients, but does not prevent their female partners from experiencing miscarriages. Notably, clinical pregnancy rates can be influenced by fertilization type, female age, and treatment year. Further studies with larger sample sizes and RCTs are needed. Future research should focus on addressing these limitations and providing more robust evidence to effectively guide clinical practice.

Acknowledgments

All authors have no acknowledgments to disclose.

Footnotes

Funding: The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: We acknowledge financial support from the Sichuan Province (No. 2024NSFSC1676) and Special Support for Postdoctoral Research Project of Sichuan Province in 2024 (No. TB2024077).

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

References

  1. Agarwal A., Sharma R. K., Sharma R., Assidi M., Abuzenadah A. M., Alshahrani S., Durairajanayagam D., Sabanegh E. (2014). Characterizing semen parameters and their association with reactive oxygen species in infertile men. Reproductive Biology and Endocrinology, 12, 33. 10.1186/1477-7827-12-33 [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Al-Mohammady A. A., El-Sherbiny A. F., Mehaney A. B., Ghobara Y. A. (2019). Varicocele repair in patients prepared for intracytoplasmic sperm injection: To do or not to do? Andrologia, 51(2), e13185. 10.1111/and.13185 [DOI] [PubMed] [Google Scholar]
  3. Ameli M., Ahmadzadeh M., Khajavi A., Nabizadeh M. (2019). Evaluation of the success rate and complications of conventional varicocelectomy: Do we need microscopic surgery really? Urologia, 86(1), 23–26. 10.1177/0391560318758938 [DOI] [PubMed] [Google Scholar]
  4. Baazeem A., Belzile E., Ciampi A., Dohle G., Jarvi K., Salonia A., Weidner W., Zini A. (2011). Varicocele and male factor infertility treatment: A new meta-analysis and review of the role of varicocele repair. European Urology, 60(4), 796–808. 10.1016/j.eururo.2011.06.018 [DOI] [PubMed] [Google Scholar]
  5. Baazeem A., Boman J. M., Libman J., Jarvi K., Zini A. (2009). Microsurgical varicocelectomy for infertile men with oligospermia: Differential effect of bilateral and unilateral varicocele on pregnancy outcomes. BJU International, 104(4), 524–528. 10.1111/j.1464-410X.2009.08431.x [DOI] [PubMed] [Google Scholar]
  6. Bhasin S., Kerr C., Oktay K., Racowsky C. (2019). The implications of reproductive aging for the health, vitality, and economic welfare of human societies. Journal of Clinical Endocrinology and Metabolism, 104(9), 3821–3825. 10.1210/jc.2019-00315 [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Binhazzaa M., Bounasr E., Perez G., Almont T., Soulie M., Faruch M., Huyghe E. (2016). Comparison of subinguinal microsurgical varicocelectomy vs percutaneous embolization in infertile men. Progres en Urologie, 26(16), 1178–1184. 10.1016/j.purol.2016.09.064 [DOI] [PubMed] [Google Scholar]
  8. Birowo P., Rahendra Wijaya J., Atmoko W., Rasyid N. (2020). The effects of varicocelectomy on the DNA fragmentation index and other sperm parameters: A meta-analysis. Basic and Clinical Andrology, 30, 15. 10.1186/s12610-020-00112-6 [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Birowo P., Tendi W., Widyahening I. S., Atmoko W., Rasyid N. (2020). The benefits of varicocele repair for achieving pregnancy in male infertility: A systematic review and meta-analysis. Heliyon, 6(11), e05439. 10.1016/j.heliyon.2020.e05439 [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Boman J. M., Libman J., Zini A. (2008). Microsurgical varicocelectomy for isolated asthenospermia. Journal of Urology, 180(5), 2129–2132. 10.1016/j.juro.2008.07.046 [DOI] [PubMed] [Google Scholar]
  11. Carson S. A., Kallen A. N. (2021). Diagnosis and management of infertility: A review. JAMA, 326(1), 65–76. 10.1001/jama.2021.4788 [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Charalambous C., Webster A., Schuh M. (2023). Aneuploidy in mammalian oocytes and the impact of maternal ageing. Nature Reviews Molecular Cell Biology, 24(1), 27–44. 10.1038/s41580-022-00517-3 [DOI] [PubMed] [Google Scholar]
  13. Cheung S., Ng L., Xie P., Kocur O., Elias R., Schlegel P., Rosenwaks Z., Palermo G. D. (2024). Genetic profiling of azoospermic men to identify the etiology and predict reproductive potential. Journal of Assisted Reproduction and Genetics, 41(4), 1111–1124. 10.1007/s10815-024-03045-5 [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Cho C. L., Esteves S. C., Agarwal A. (2016). Novel insights into the pathophysiology of varicocele and its association with reactive oxygen species and sperm DNA fragmentation. Asian Journal of Andrology, 18(2), 186–193. 10.4103/1008-682x.170441 [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Chung K. L. Y., Hung J. W. S., Yam F. S. D., Chao N. S. Y., Li D. C. Y., Leung M. W. Y. (2023). Prospective randomized controlled trial comparing laparoscopic palomo surgery vs scrotal antegrade sclerotherapy in adolescent varicocele. Journal of Urology, 209(3), 600–610. 10.1097/ju.0000000000003087 [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Cioppi F., Rosta V., Krausz C. (2021). Genetics of azoospermia. International Journal of Molecular Sciences, 22(6), 3264. 10.3390/ijms22063264 [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Daitch J. A., Bedaiwy M. A., Pasqualotto E. B., Hendin B. N., Hallak J., Falcone T., Thomas A. J., Nelson D. R., Agarwal A. (2001). Varicocelectomy improves intrauterine insemination success rates in men with varicocele. Journal of Urology, 165(5), 1510–1513. [PubMed] [Google Scholar]
  18. du Fossé N. A., van der Hoorn M. P., van Lith J. M. M., le Cessie S., Lashley E. (2020). Advanced paternal age is associated with an increased risk of spontaneous miscarriage: A systematic review and meta-analysis. Human Reproduction Update, 26(5), 650–669. 10.1093/humupd/dmaa010 [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Dubin J. M., Greer A. B., Kohn T. P., Masterson T. A., Ji L., Ramasamy R. (2018). Men with severe oligospermia appear to benefit from varicocele repair: A cost-effectiveness analysis of assisted reproductive technology. Urology, 111, 99–103. 10.1016/j.urology.2017.10.010 [DOI] [PubMed] [Google Scholar]
  20. Esteves S. C., Oliveira F. V., Bertolla R. P. (2010). Clinical outcome of intracytoplasmic sperm injection in infertile men with treated and untreated clinical varicocele. Journal of Urology, 184(4), 1442–1446. 10.1016/j.juro.2010.06.004 [DOI] [PubMed] [Google Scholar]
  21. Garolla A., Torino M., Miola P., Caretta N., Pizzol D., Menegazzo M., Bertoldo A., Foresta C. (2015). Twenty-four-hour monitoring of scrotal temperature in obese men and men with a varicocele as a mirror of spermatogenic function. Human Reproduction, 30(5), 1006–1013. 10.1093/humrep/dev057 [DOI] [PubMed] [Google Scholar]
  22. Gokce M. I., Gulpinar O., Suer E., Mermerkaya M., Aydos K., Yaman O. (2013). Effect of performing varicocelectomy before intracytoplasmic sperm injection on clinical outcomes in non-azoospermic males. International Urology and Nephrology, 45(2), 367–372. 10.1007/s11255-013-0394-2 [DOI] [PubMed] [Google Scholar]
  23. Goldstein M., Eid J. F. (1989). Elevation of intratesticular and scrotal skin surface temperature in men with varicocele. Journal of Urology, 142(3), 743–745. 10.1016/s0022-5347(17)38874-2 [DOI] [PubMed] [Google Scholar]
  24. Gourinat A., Mazeaud C., Hubert J., Eschwege P., Koscinski I. (2023). Impact of paternal age on assisted reproductive technology outcomes and offspring health: A systematic review. Andrology, 11(6), 973–986. 10.1111/andr.13385 [DOI] [PubMed] [Google Scholar]
  25. Haydardedeoglu B., Turunc T., Kilicdag E. B., Gul U., Bagis T. (2010). The effect of prior varicocelectomy in patients with nonobstructive azoospermia on intracytoplasmic sperm injection outcomes: A retrospective pilot study. Urology, 75(1), 83–86. 10.1016/j.urology.2009.09.023 [DOI] [PubMed] [Google Scholar]
  26. Huan L., Hao D., Jun Z., Wen-Min M. (2019). Outcome of artificial insemination after Palomo varicoceletomy with preserving artery. Journal of Reproductive Medicine, 28(8), 911–914. https://doi.org/10.3969/j.issn.1004–3845. [Google Scholar]
  27. Inci K., Hascicek M., Kara O., Dikmen A. V., Gurgan T., Ergen A. (2009). Sperm retrieval and intracytoplasmic sperm injection in men with nonobstructive azoospermia, and treated and untreated varicocele. Journal of Urology, 182(4), 1500–1505. 10.1016/j.juro.2009.06.028 [DOI] [PubMed] [Google Scholar]
  28. Inhorn M. C., Patrizio P. (2015). Infertility around the globe: New thinking on gender, reproductive technologies and global movements in the 21st century. Human Reproduction Update, 21(4), 411–426. 10.1093/humupd/dmv016 [DOI] [PubMed] [Google Scholar]
  29. Jellad S., Hammami F., Khalbous A., Messousi M., Khiari R., Ghozzi S., Chibani M. (2021). Sperm DNA status in infertile patients with clinical varicocele. Progrès en Urologie, 31(2), 105–111. 10.1016/j.purol.2020.07.241 [DOI] [PubMed] [Google Scholar]
  30. Jensen C. F. S., Østergren P., Dupree J. M., Ohl D. A., Sønksen J., Fode M. (2017). Varicocele and male infertility. Nature Reviews Urology, 14(9), 523–533. 10.1038/nrurol.2017.98 [DOI] [PubMed] [Google Scholar]
  31. Jiang W., Zhu L., Gao L., Wang J., Fang J., Chen L., Wang S. (2024). What sperm parameters effect blastocyst formation and quality during ICSI with severe male infertility. Systems Biology in Reproductive Medicine, 70(1), 218–227. 10.1080/19396368.2024.2375710 [DOI] [PubMed] [Google Scholar]
  32. Johnson D., Sandlow J. (2017). Treatment of varicoceles: Techniques and outcomes. Fertility and Sterility, 108(3), 378–384. 10.1016/j.fertnstert.2017.07.020 [DOI] [PubMed] [Google Scholar]
  33. Ketabchi A. A., Salehi S., Salajghah S. (2018). The effect of varicocelectomy on assisted reproductive technique indications and outcomes based on Kruger strict morphology test: A randomized clinical trial. Journal of Kerman University of Medical Sciences, 25(6), 519–527. [Google Scholar]
  34. Kirby E. W., Wiener L. E., Rajanahally S., Crowell K., Coward R. M. (2016). Undergoing varicocele repair before assisted reproduction improves pregnancy rate and live birth rate in azoospermic and oligospermic men with a varicocele: A systematic review and meta-analysis. Fertility and Sterility, 106(6), 1338–1343. 10.1016/j.fertnstert.2016.07.1093 [DOI] [PubMed] [Google Scholar]
  35. Kohn J. R., Haney N. M., Nichols P. E., Rodriguez K. M., Kohn T. P. (2020). Varicocele repair prior to assisted reproductive technology: Patient selection and special considerations. Research and Reports in Urology, 12, 149–156. 10.2147/RRU.S198934 [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Kohn T. P., Kohn J. R., Pastuszak A. W. (2017). Varicocelectomy before assisted reproductive technology: Are outcomes improved? Fertility and Sterility, 108(3), 385–391. 10.1016/j.fertnstert.2017.06.033 [DOI] [PubMed] [Google Scholar]
  37. Lahoz Alonso R., Sienes Bailo P., César Márquez M., Sánchez Torres J. C., Albericio Portero J. I., Sánchez Parrilla M., Suárez Broto M. A., Rello Varas L., Izquierdo Álvarez S. (2023). AZF gene microdeletions in azoospermic-oligozoospermic males. Medicina Clínica, 160(4), 151–155. 10.1016/j.medcli.2022.06.016 [DOI] [PubMed] [Google Scholar]
  38. Li H., Nawsherwan Fan C., Mubarik S., Nabi G., Ping Y. X. (2022). The trend in delayed childbearing and its potential consequences on pregnancy outcomes: A single center 9-years retrospective cohort study in Hubei, China. BMC Pregnancy Childbirth, 22(1), 514. 10.1186/s12884-022-04807-8 [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Li X., Yang X., Wang X., Wang L., Liu J., Cai F., Wang Y., Lu S. (2020). Comparison of outcomes in intrauterine insemination, in vitro fertilisation and intracytoplasmic sperm injection in men with and without varicocele. International Journal of Medical Sciences, 17(14), 2155–2162. 10.7150/ijms.48005 [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Lin H., Li Y., Ou S., Jiao X., Wang W., Haahr T., Humaidan P., Zhang Q. (2022). The relationship of total progressive motile sperm count with the outcome of IUI? An analysis of 5171 cycles. Gynecological Endocrinology, 38(11), 954–959. 10.1080/09513590.2022.2126453 [DOI] [PubMed] [Google Scholar]
  41. Lin H., Li Y., Ou S., Jiao X., Wang W., Humaidan P., Zhang Q. (2021). Role of the total progressive motile sperm count (TPMSC) in different infertility factors in IUI: A retrospective cohort study. BMJ Open, 11(2), e040563. 10.1136/bmjopen-2020-040563 [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Marmar J. L., Corson S. L., Batzer F. R., Gocial B. (1992). Insemination data on men with varicoceles. Fertility and Sterility, 57(5), 1084–1090. 10.1016/s0015-0282(16)55028-6 [DOI] [PubMed] [Google Scholar]
  43. Mikwar M., MacFarlane A. J., Marchetti F. (2020). Mechanisms of oocyte aneuploidy associated with advanced maternal age. Mutation Research—Reviews in Mutation Research, 785, 108320. 10.1016/j.mrrev.2020.108320 [DOI] [PubMed] [Google Scholar]
  44. Mostafa T., Anis T., Imam H., El-Nashar A. R., Osman I. A. (2009). Seminal reactive oxygen species-antioxidant relationship in fertile males with and without varicocele. Andrologia, 41(2), 125–129. 10.1111/j.1439-0272.2008.00900.x [DOI] [PubMed] [Google Scholar]
  45. Motta A., Caltabiano G., Pizzarelli M., Failla G., Botezatu D., Muresanu H., Foti P., La Vignera S., Condorelli R., Palmucci S., Basile A. (2019). Varicocele, conventional laparoscopic ligation versus occluding balloon embolization. Radiologia Medica, 124(5), 438–443. 10.1007/s11547-018-0968-2 [DOI] [PubMed] [Google Scholar]
  46. Nabi G., Asterlings S., Greene D. R., Marsh R. L. (2004). Percutaneous embolization of varicoceles: Outcomes and correlation of semen improvement with pregnancy. Urology, 63(2), 359–363. 10.1016/j.urology.2003.09.026 [DOI] [PubMed] [Google Scholar]
  47. Nakonechnyi Y., Nakonechnyi A., Fraczek M., Havrylyuk A., Kamieniczna M., Chopyak V., Kurpisz M. (2022). Varicocelectomy improves sperm parameters, sperm DNA integrity as well as the other critical semen features. Journal of Physiology and Pharmacology, 73(6). 10.26402/jpp.2022.6.09 [DOI] [PubMed] [Google Scholar]
  48. O’Brien J. H., Bowles B., Kamal K. M., Jarvi K., Zini A. (2004). Microsurgical varicocelectomy for infertile couples with advanced female age: Natural history in the era of ART. Journal of Andrology, 25(6), 939–943. 10.1002/j.1939-4640.2004.tb03165.x [DOI] [PubMed] [Google Scholar]
  49. Pasqualotto F. F., Braga D. P., Figueira R. C., Setti A. S., Iaconelli A., Jr., Borges E., Jr. (2012). Varicocelectomy does not impact pregnancy outcomes following intracytoplasmic sperm injection procedures. Journal of Andrology, 33(2), 239–243. 10.2164/jandrol.110.011932 [DOI] [PubMed] [Google Scholar]
  50. Pasqualotto F. F., Lucon A. M., Hallak J., Góes P. M., Saldanha L. B., Arap S. (2003). Induction of spermatogenesis in azoospermic men after varicocele repair. Human Reproduction, 18(1), 108–112. 10.1093/humrep/deg032 [DOI] [PubMed] [Google Scholar]
  51. Peng J., Zhang Z., Cui W., Yuan Y., Song W., Gao B., Xin Z., Zhu S. (2015). Spontaneous pregnancy rates in Chinese men undergoing microsurgical subinguinal varicocelectomy and possible preoperative factors affecting the outcomes. Fertility and Sterility, 103(3), 635–639. 10.1016/j.fertnstert.2014.12.091 [DOI] [PubMed] [Google Scholar]
  52. Ribeiro S., Sousa M. (2023). In vitro fertilisation and intracytoplasmic sperm injection predictive factors: A review of the effect of female age, ovarian reserve, male age, and male factor on IVF/ICSI treatment outcomes. JBRA Assisted Reproduction, 27(1), 97–111. 10.5935/1518-0557.20220000 [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Santana V. P., Miranda-Furtado C. L., Pedroso D. C. C., Eiras M. C., Vasconcelos M. A. C., Ramos E. S., Calado R.T., Ferriani R.A., Esteves S.C., Dos Reis R. M. (2019). The relationship among sperm global DNA methylation, telomere length, and DNA fragmentation in varicocele: A cross-sectional study of 20 cases. Systems Biology in Reproductive Medicine, 65(2), 95–104. 10.1080/19396368.2018.1557762 [DOI] [PubMed] [Google Scholar]
  54. Sepúlveda L., Coimbra D., Lourenço M., Santos L., Oliveira C., Coutinho S., Ramos M. (2018). Varicocele treatment in patients up to 35 years old: A multicentric retrospective studycomparing 3 different techniques. Archivos Espanoles de Urologia, 71(6), 543–548. [PubMed] [Google Scholar]
  55. Soetandar A., Noegroho B. S., Siregar S., Adriansjah R., Mustafa A. (2022). Microsurgical varicocelectomy effects on sperm DNA fragmentation and sperm parameters in infertile male patients: A systematic review and meta-analysis of more recent evidence. Archivio Italiano di Urologia e Andrologia, 94(3), 360–365. 10.4081/aiua.2022.3.360 [DOI] [PubMed] [Google Scholar]
  56. Sonmez M. G., Haliloglu A. H. (2018). Role of varicocele treatment in assisted reproductive technologies. Arab Journal of Urology, 16(1), 188–196. 10.1016/j.aju.2018.01.002 [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Taniguchi M., Kanasaki H., Oride A., Okada H., Imamura K., Kyo S. (2024). Impact of current and previous sperm findings on outcomes of intrauterine insemination. Reproductive Medicine and Biology, 23(1), e12574. 10.1002/rmb2.12574 [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Vasconcelos A. L., Campbell M. J., Barratt C. L. R., Gellatly S. A. (2022). Do studies published in two leading reproduction journals between 2011 and 2020 demonstrate that they followed WHO5 recommendations for basic semen analysis? Human Reproduction, 37(10), 2255–2263. 10.1093/humrep/deac173 [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Wang Q., Yu Y., Liu Y., Wang L. (2019). Outcome of varicocelectomy on different degrees of total motile sperm count: A systematic review and meta-analysis. Systems Biology in Reproductive Medicine, 65(6), 430–436. 10.1080/19396368.2019.1655813 [DOI] [PubMed] [Google Scholar]
  60. Zhang F., Dai M., Yang X., Cheng Y., Ye L., Huang W., Chen X., Yin T., Sha Y. (2024). Predictors of successful salvage microdissection testicular sperm extraction (mTESE) after failed initial TESE in patients with non-obstructive azoospermia: A systematic review and meta-analysis. Andrology, 12(1), 30–44. 10.1111/andr.13448 [DOI] [PubMed] [Google Scholar]
  61. Zhang X. Z., Yao K. S., Xiong C. L. (2011). A comparative study of sperm morphology evaluation criteria by the fifth and fourth editions of WHO laboratory manual. Zhonghua Nan Ke Xue, 17(11), 989–992. [PubMed] [Google Scholar]
  62. Zhang Y., Zhang W., Wu X., Liu G., Dai Y., Jiang H., Zhang X. (2022). Effect of varicocele on sperm DNA damage: A systematic review and meta-analysis. Andrologia, 54(1), e14275. 10.1111/and.14275 [DOI] [PubMed] [Google Scholar]
  63. Zini A., Boman J., Baazeem A., Jarvi K., Libman J. (2008). Natural history of varicocele management in the era of intracytoplasmic sperm injection. Fertility and Sterility, 90(6), 2251–2256. 10.1016/j.fertnstert.2007.10.071 [DOI] [PubMed] [Google Scholar]

Articles from American Journal of Men's Health are provided here courtesy of SAGE Publications

RESOURCES