Consensus and Diversity in the Management of Varicocele for Male Infertility: Results of a Global Practice Survey and Comparison with Guidelines and Recommendations

Rupin Shah 1, Ashok Agarwal 2, Parviz Kavoussi 3, Amarnath Rambhatla 4, Ramadan Saleh 5, Rossella Cannarella 6, Ahmed M Harraz 7 8 9, Florence Boitrelle 10 11, Shinnosuke Kuroda 12, Taha Abo-Almagd Abdel-Meguid Hamoda 13 14, Armand Zini 15, Edmund Ko 16, Gokhan Calik 17, Tuncay Toprak 18, Hussein Kandil 19, Murat Gül 20, Mustafa Emre Bakırcıoğlu 21, Neel Parekh 22, Giorgio Ivan Russo 23, Nicholas Tadros 24, Ates Kadioglu 25, Mohamed Arafa 12 26 27, Eric Chung 28, Osvaldo Rajmil 29, Fotios Dimitriadis 30, Vineet Malhotra 31, Gianmaria Salvio 32, Ralf Henkel 33 34, Tan V Le 35 36, Emrullah Sogutdelen 37, Sarah Vij 22, Abdullah Alarbid 8, Ahmet Gudeloglu 38, Akira Tsujimura 39, Aldo E Calogero 6, Amr El Meliegy 40, Andrea Crafa 6, Arif Kalkanli 41, Aykut Baser 42, Berk Hazir 43, Carlo Giulioni 44, Chak-Lam Cho 45, Christopher C K Ho 46, Ciro Salzano 47, Daniel Suslik Zylbersztejn 48, Dung Mai Ba Tien 35, Edoardo Pescatori 49, Edson Borges 50, Ege Can Serefoglu 51, Emine Saïs-Hamza 10 11, Eric Huyghe 52, Erman Ceyhan 53, Ettore Caroppo 54, Fabrizio Castiglioni 55, Fahmi Bahar 56, Fatih Gokalp 57, Francesco Lombardo 58, Franco Gadda 59, Gede Wirya Kusuma Duarsa 60, Germar-Michael Pinggera 61, Gian Maria Busetto 62, Giancarlo Balercia 32, Gianmartin Cito 63, Gideon Blecher 64 65, Giorgio Franco 66, Giovanni Liguori 67, Haitham Elbardisi 26 68, Hakan Keskin 38, Haocheng Lin 69, Hisanori Taniguchi 70, Hyun Jun Park 71 72, Imad Ziouziou 73, Jean de la Rosette 74, Jim Hotaling 75, Jonathan Ramsay 76, Juan Manuel Corral Molina 77, Ka Lun Lo 78, Kadir Bocu 79, Kareim Khalafalla 26 80, Kasonde Bowa 81, Keisuke Okada 82, Koichi Nagao 83, Koji Chiba 82, Lukman Hakim 84, Konstantinos Makarounis 85, Marah Hehemann 86, Marcelo Rodriguez Peña 87, Marco Falcone 88, Marion Bendayan 10 11, Marlon Martinez 89, Massimiliano Timpano 88, Mesut Altan 90, Mikkel Fode 91 92, Mohamed S Al-Marhoon 93, Mohammad Ali Sadighi Gilani 94, Mohammad Ayodhia Soebadi 95, Nazim Gherabi 96, Nikolaos Sofikitis 97, Oğuzhan Kahraman 53, Ponco Birowo 98, Priyank Kothari 99, Puneet Sindhwani 100, Qaisar Javed 101, Rafael F Ambar 102 103, Raghavender Kosgi 104, Ramy Abou Ghayda 105, Ricky Adriansjah 106, Rosita Angela Condorelli 6, Sandro La Vignera 6, Sava Micic 107, Shannon Hee Kyung Kim 108 109, Shinichiro Fukuhara 110, Sun Tae Ahn 111, Taymour Mostafa 40, Teng Aik Ong 112, Teppei Takeshima 113, Toshiyasu Amano 114, Trenton Barrett 115, Umut Arslan 18, Vilvapathy Senguttuvan Karthikeyan 116, Widi Atmoko 104, Yasushi Yumura 113, Yiming Yuan 117, Yuki Kato 118, Davor Jezek 119, Bryan Kwun-Chung Cheng 120, Georgios Hatzichristodoulou 121, Jun Dy 122, Eduard Ruiz Castañé 123, Ahmed I El-Sakka 124, Quang Nguyen 125 126, Selcuk Sarikaya 127, Luca Boeri 59, Ronny Tan 128 129, Mohamad A Moussa 130 131, Ahmed El-Assmy 7, Hamed Alali 132, Naif Alhathal 133, Yasser Osman 7, Dragoljub Perovic 134, Hesamoddin Sajadi 99, Hamed Akhavizadegan 135, Miroslav Vučinić 136, Said Kattan 133, Mohamed S Kattan 133, Nasser Mogharabian 137, Nguyen Ho Vinh Phuoc 35, Kay Seong Ngoo 138, Mohammad H Alkandari 139, Shaheed Alsuhaibani 140, Ioannis Sokolakis 121, Mehdi Babaei 141, Mak Siu King 78, Thorsten Diemer 142, Marcelo M Gava 102 103, Raphael Henrique 143, Rodrigo Spinola E Silva 102 103, Gustavo Marquesine Paul 144, Tiago Cesar Mierzwa 145, Sidney Glina 102, Kashif Siddiqi 146, Han Wu 147, Jana Wurzacher 148, Ala'a Farkouh 12, Hwancheol Son 149, Suks Minhas 150, Joe Lee 151, Nikko Magsanoc 152, Paolo Capogrosso 153, German Jose Albano 89, Sheena E M Lewis 154, Channa N Jayasena 155 156, Juan G Alvarez 157, Colin Teo 158, Ryan P Smith 159, Jo Ben M Chua 160, Christian Fuglesang S Jensen 161, Sijo Parekattil 162, Renata Finelli 12, Damayanthi Durairajanayagam 163, Keshab Kumar Karna 12, Abdelkareem Ahmed 9, Don Evenson 164, Yukihiro Umemoto 165, Ana Puigvert 166, Gökhan Çeker 167 168, Giovanni M Colpi 169; Global Andrology Forum

Affiliations

01 January 2023

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doi: 10.5534/wjmh.220048

Abstract

Purpose: Varicocele is a common problem among infertile men. Varicocele repair (VR) is frequently performed to improve semen parameters and the chances of pregnancy. However, there is a lack of consensus about the diagnosis, indications for VR and its outcomes. The aim of this study was to explore global practice patterns on the management of varicocele in the context of male infertility.

Materials and methods: Sixty practicing urologists/andrologists from 23 countries contributed 382 multiple-choice-questions pertaining to varicocele management. These were condensed into an online questionnaire that was forwarded to clinicians involved in male infertility management through direct invitation. The results were analyzed for disagreement and agreement in practice patterns and, compared with the latest guidelines of international professional societies (American Urological Association [AUA], American Society for Reproductive Medicine [ASRM], and European Association of Urology [EAU]), and with evidence emerging from recent systematic reviews and meta-analyses. Additionally, an expert opinion on each topic was provided based on the consensus of 16 experts in the field.

Results: The questionnaire was answered by 574 clinicians from 59 countries. The majority of respondents were urologists/uro-andrologists. A wide diversity of opinion was seen in every aspect of varicocele diagnosis, indications for repair, choice of technique, management of sub-clinical varicocele and the role of VR in azoospermia. A significant proportion of the responses were at odds with the recommendations of AUA, ASRM, and EAU. A large number of clinical situations were identified where no guidelines are available.

Conclusions: This study is the largest global survey performed to date on the clinical management of varicocele for male infertility. It demonstrates: 1) a wide disagreement in the approach to varicocele management, 2) large gaps in the clinical practice guidelines from professional societies, and 3) the need for further studies on several aspects of varicocele management in infertile men.

Keywords: Consensus; Disease management; Male infertility; Survey; Varicocele.

Conflict of interest statement

The authors have nothing to disclose.

Figures

Fig. 1. Geographical distribution of respondents. The number of respondents is shown in brackets after the name of each country. The violet color indicates the country with the greatest number of respondents (n=105), the blue color are those with a lower number (n=59), the orange color are those with a further reduction in the number of respondents (from 26 to 38), and the yellow color are the countries with the lowest number of respondents (from 1 to 17).

Fig. 1. Geographical distribution of respondents. The number of respondents is shown in brackets after the name of each country. The violet color indicates the country with the greatest number of respondents (n=105), the blue color are those with a lower number (n=59), the orange color are those with a further reduction in the number of respondents (from 26 to 38), and the yellow color are the countries with the lowest number of respondents (from 1 to 17).

Fig. 2. Number of varicocele repairs (VRs) done annually by the respondents.

Fig. 2. Number of varicocele repairs (VRs) done annually by the respondents.

Fig. 3. Degree of agreement of the respondents with the premise of the survey.

Fig. 3. Degree of agreement of the respondents with the premise of the survey.

Fig. 4. Estimated percentage of patients presenting with common symptoms related to varicocele.

Fig. 4. Estimated percentage of patients presenting with common symptoms related to varicocele.

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References

  1.  
    1. Su JS, Farber NJ, Vij SC. Pathophysiology and treatment options of varicocele: an overview. Andrologia. 2021;53:e13576. - PubMed
  2.  
    1. Alsaikhan B, Alrabeeah K, Delouya G, Zini A. Epidemiology of varicocele. Asian J Androl. 2016;18:179–181. - PMC - PubMed
  3.  
    1. Damsgaard J, Joensen UN, Carlsen E, Erenpreiss J, Blomberg Jensen M, Matulevicius V, et al. Varicocele is associated with impaired semen quality and reproductive hormone levels: a study of 7035 healthy young men from six European countries. Eur Urol. 2016;70:1019–1029. - PubMed
  4.  
    1. World Health Organization. The influence of varicocele on parameters of fertility in a large group of men presenting to infertility clinics. Fertil Steril. 1992;57:1289–1293. - PubMed
  5.  
    1. Baskaran S, Agarwal A, Leisegang K, Pushparaj PN, Panner Selvam MK, Henkel R. An in-depth bibliometric analysis and current perspective on male infertility research. World J Mens Health. 2021;39:302–314. - PMC - PubMed
  6.  
    1. Agarwal A, Finelli R, Durairajanayagam D, Leisegang K, Henkel R, Salvio G, et al. Comprehensive analysis of global research on human varicocele: a scientometric approach. World J Mens Health. 2022 doi: 10.5534/wjmh.210202. [Epub] - DOI - PMC - PubMed
  7.  
    1. Persad E, O'Loughlin CA, Kaur S, Wagner G, Matyas N, Hassler-Di Fratta MR, et al. Surgical or radiological treatment for varicoceles in subfertile men. Cochrane Database Syst Rev. 2021;4:CD000479. - PMC - PubMed
  8.  
    1. Salonia A, Bettocchi C, Boeri L, Capogrosso P, Carvalho J, Cilesiz NC, et al. EAU Working Group on Male Sexual and Reproductive Health. European Association of Urology guidelines on sexual and reproductive health-2021 update: male sexual dysfunction. Eur Urol. 2021;80:333–357. - PubMed
  9.  
    1. Minhas S, Bettocchi C, Boeri L, Capogrosso P, Carvalho J, Cilesiz NC, et al. EAU Working Group on Male Sexual and Reproductive Health. European Association of Urology guidelines on male sexual and reproductive health: 2021 update on male infertility. Eur Urol. 2021;80:603–620. - PubMed
  10.  
    1. Schlegel PN, Sigman M, Collura B, De Jonge CJ, Eisenberg ML, Lamb DJ, et al. Diagnosis and treatment of infertility in men: AUA/ASRM guideline. Linthicum (MD): American Urology Association; 2020.
  11.  
    1. Schlegel PN, Sigman M, Collura B, De Jonge CJ, Eisenberg ML, Lamb DJ, et al. Diagnosis and treatment of infertility in men: AUA/ASRM guideline part I. J Urol. 2021;205:36–43. - PubMed
  12.  
    1. Schlegel PN, Sigman M, Collura B, De Jonge CJ, Eisenberg ML, Lamb DJ, et al. Diagnosis and treatment of infertility in men: AUA/ASRM guideline part II. J Urol. 2021;205:44–51. - PubMed
  13.  
    1. Freeman S, Bertolotto M, Richenberg J, Belfield J, Dogra V, Huang DY, et al. members of the ESUR-SPIWG WG. Ultrasound evaluation of varicoceles: guidelines and recommendations of the European Society of Urogenital Radiology Scrotal and Penile Imaging Working Group (ESUR-SPIWG) for detection, classification, and grading. Eur Radiol. 2020;30:11–25. - PubMed
  14.  
    1. Hoekstra T, Witt MA. The correlation of internal spermatic vein palpability with ultrasonographic diameter and reversal of venous flow. J Urol. 1995;153:82–84. - PubMed
  15.  
    1. Pilatz A, Altinkilic B, Kohler E, Marconi M, Weidner W. Color Doppler ultrasound imaging in varicoceles: is the venous diameter sufficient for predicting clinical and subclinical varicocele? World J Urol. 2011;29:645–650. - PubMed
  16.  
    1. Karami M, Mazdak H, Khanbabapour S, Adibi A, Nasr N. Determination of the best position and site for color Doppler ultrasonographic evaluation of the testicular vein to define the clinical grades of varicocele ultrasonographically. Adv Biomed Res. 2014;3:17. - PMC - PubMed
  17.  
    1. Cavallini G, Scroppo FI, Colpi GM. The clinical usefulness of a novel grading system for varicocoeles using duplex Doppler ultrasound examination based on postsurgical modifications of seminal parameters. Andrology. 2019;7:62–68. - PubMed
  18.  
    1. An AUA Best Practice Policy, ASRM Practice Committee Report. Report on varicocele and infertility [Internet] Linthicum (MD): American Urological Association; 2012. [Cited 2022 May 27]. Available from: https://www.auanet.org/documents/education/clinical-guidance/Varicocele-... .
  19.  
    1. Pyrgidis N, Sokolakis I, Palapelas V, Tishukov M, Mykoniatis I, Symeonidis EN, et al. The effect of antioxidant supplementation on operated or non-operated varicocele-associated infertility: a systematic review and meta-analysis. Antioxidants (Basel) 2021;10:106. - PMC - PubMed
  20.  
    1. Giagulli VA, Carbone MD. Varicocele correction for infertility: which patients to treat? Int J Androl. 2011;34:236–241. - PubMed
  21.  
    1. Nieschlag E, Hertle L, Fischedick A, Abshagen K, Behre HM. Update on treatment of varicocele: counselling as effective as occlusion of the vena spermatica. Hum Reprod. 1998;13:2147–2150. - PubMed
  22.  
    1. Wang Q, Yu Y, Liu Y, Wang L. Outcome of varicocelectomy on different degrees of total motile sperm count: a systematic review and meta-analysis. Syst Biol Reprod Med. 2019;65:430–436. - PubMed
  23.  
    1. Boman JM, Libman J, Zini A. Microsurgical varicocelectomy for isolated asthenospermia. J Urol. 2008;180:2129–2132. - PubMed
  24.  
    1. Cakiroglu B, Sinanoglu O, Gozukucuk R. The effect of varicocelectomy on sperm parameters in subfertile men with clinical varicoceles who have asthenozoospermia or teratozoospermia with normal sperm density. ISRN Urol. 2013;2013:698351. - PMC - PubMed
  25.  
    1. Okeke L, Ikuerowo O, Chiekwe I, Etukakpan B, Shittu O, Olapade-Olaopa O. Is varicocelectomy indicated in subfertile men with clinical varicoceles who have asthenospermia or teratospermia and normal sperm density? Int J Urol. 2007;14:729–732. - PubMed
  26.  
    1. Coetzee K, Kruge TF, Lombard CJ. Predictive value of normal sperm morphology: a structured literature review. Hum Reprod Update. 1998;4:73–82. - PubMed
  27.  
    1. Danis RB, Samplaski MK. Sperm morphology: history, challenges, and impact on natural and assisted fertility. Curr Urol Rep. 2019;20:43. - PubMed
  28.  
    1. Kohn TP, Kohn JR, Ramasamy R. Effect of sperm morphology on pregnancy success via intrauterine insemination: a systematic review and meta-analysis. J Urol. 2018;199:812–822. - PubMed
  29.  
    1. Choe JH, Seo JT. Is varicocelectomy useful for subfertile men with isolated teratozoospermia? Urology. 2015;86:1123–1128. - PubMed
  30.  
    1. Ilktac A, Hamidli S, Ersoz C, Dogan B, Akcay M. Efficacy of varicocelectomy in primary infertile patients with isolated teratozoospermia. A retrospective analysis. Andrologia. 2020;52:e13875. - PubMed
  31.  
    1. Cakan M, Bakirtas H, Aldemir M, Demirel F, Altug U. Results of varicocelectomy in patients with isolated teratozoospermia. Urol Int. 2008;80:172–176. - PubMed
  32.  
    1. De Braekeleer M, Nguyen MH, Morel F, Perrin A. Genetic aspects of monomorphic teratozoospermia: a review. J Assist Reprod Genet. 2015;32:615–623. - PMC - PubMed
  33.  
    1. Dumont A, Barbotin AL, Lefebvre-Khalil V, Mitchell V, Rigot JM, Boitrelle F, et al. [Necrozoospermia: from etiologic diagnosis to therapeutic management] Gynecol Obstet Fertil Senol. 2017;45:238–248. French. - PubMed
  34.  
    1. Ribas-Maynou J, Yeste M, Becerra-Tomas N, Aston KI, James ER, Salas-Huetos A. Clinical implications of sperm DNA damage in IVF and ICSI: updated systematic review and meta-analysis. Biol Rev Camb Philos Soc. 2021;96:1284–1300. - PubMed
  35.  
    1. Lara-Cerrillo S, Gual-Frau J, Benet J, Abad C, Prats J, Amengual MJ, et al. Microsurgical varicocelectomy effect on sperm telomere length, DNA fragmentation and seminal parameters. Hum Fertil (Camb) 2022;25:135–141. - PubMed
  36.  
    1. Lira Neto FT, Roque M, Esteves SC. Effect of varicocelectomy on sperm deoxyribonucleic acid fragmentation rates in infertile men with clinical varicocele: a systematic review and meta-analysis. Fertil Steril. 2021;116:696–712. - PubMed
  37.  
    1. Qiu D, Shi Q, Pan L. Efficacy of varicocelectomy for sperm DNA integrity improvement: a meta-analysis. Andrologia. 2021;53:e13885. - PubMed
  38.  
    1. Saleh RA, Agarwal A, Sharma RK, Said TM, Sikka SC, Thomas AJ., Jr Evaluation of nuclear DNA damage in spermatozoa from infertile men with varicocele. Fertil Steril. 2003;80:1431–1436. - PubMed
  39.  
    1. Smith R, Kaune H, Parodi D, Madariaga M, Rios R, Morales I, et al. Increased sperm DNA damage in patients with varicocele: relationship with seminal oxidative stress. Hum Reprod. 2006;21:986–993. - PubMed
  40.  
    1. Ammar O, Tekeya O, Hannachi I, Sallem A, Haouas Z, Mehdi M. Increased sperm DNA fragmentation in infertile men with varicocele: relationship with apoptosis, seminal oxidative stress, and spermatic parameters. Reprod Sci. 2021;28:909–919. - PubMed
  41.  
    1. Jeremias JT, Belardin LB, Okada FK, Antoniassi MP, Fraietta R, Bertolla RP, et al. Oxidative origin of sperm DNA fragmentation in the adult varicocele. Int Braz J Urol. 2021;47:275–283. - PMC - PubMed
  42.  
    1. Fathi A, Mohamed O, Mahmoud O, Alsagheer GA, Reyad AM, Abolyosr A, et al. The impact of varicocelectomy on sperm DNA fragmentation and pregnancy rate in subfertile men with normal semen parameters: a pilot study. Arab J Urol. 2021;19:186–190. - PMC - PubMed
  43.  
    1. Esteves SC, Roque M, Agarwal A. Outcome of assisted reproductive technology in men with treated and untreated varicocele: systematic review and meta-analysis. Asian J Androl. 2016;18:254–258. - PMC - PubMed
  44.  
    1. Kirby EW, Wiener LE, Rajanahally S, Crowell K, Coward RM. 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. Fertil Steril. 2016;106:1338–1343. - PubMed
  45.  
    1. Tan TY, Lau SK, Loh SF, Tan HH. Female ageing and reproductive outcome in assisted reproduction cycles. Singapore Med J. 2014;55:305–309. - PMC - PubMed
  46.  
    1. Fırat F, Erdemir F. The effect of age on semen quality and spontaneous pregnancy rates in patients who treated with microsurgical inguinal varicocelectomy. Cureus. 2020;12:e7744. - PMC - PubMed
  47.  
    1. Hsiao W, Rosoff JS, Pale JR, Greenwood EA, Goldstein M. Older age is associated with similar improvements in semen parameters and testosterone after subinguinal microsurgical varicocelectomy. J Urol. 2011;185:620–625. - PubMed
  48.  
    1. Asafu-Adjei D, Judge C, Deibert CM, Li G, Stember D, Stahl PJ. Systematic review of the impact of varicocele grade on response to surgical management. J Urol. 2020;203:48–56. - PubMed
  49.  
    1. Birowo P, Prasetyo DT, Pujianto DA, Atmoko W, Rasyid N, Sini IR. Effect of varicocele repair on sperm retrieval rate and testicular histopathological patterns in men with nonobstructive azoospermia. Asian J Androl. 2022;24:85–89. - PMC - PubMed
  50.  
    1. Cantoro U, Catanzariti F, Lacetera V, Quaresima L, Giovanni M, Polito M. Percentage change of FSH value: new variable to predict the seminal outcome after varicocelectomy. Andrologia. 2015;47:412–416. - PubMed
  51.  
    1. Zhou T, Zhang W, Chen Q, Li L, Cao H, Xu CL, et al. Effect of varicocelectomy on testis volume and semen parameters in adolescents: a meta-analysis. Asian J Androl. 2015;17:1012–1016. - PMC - PubMed
  52.  
    1. Culha M, Mutlu N, Acar O, Baykal M. Comparison of testicular volumes before and after varicocelectomy. Urol Int. 1998;60:220–223. - PubMed
  53.  
    1. Sakamoto H, Saito K, Ogawa Y, Yoshida H. Effects of varicocele repair in adults on ultrasonographically determined testicular volume and on semen profile. Urology. 2008;71:485–489. - PubMed
  54.  
    1. Almekaty K, Zahran MH, Zoeir A, Minhas S, Salem K. The role of artery-preserving varicocelectomy in subfertile men with severe oligozoospermia: a randomized controlled study. Andrology. 2019;7:193–198. - PubMed
  55.  
    1. Majzoub A, ElBardisi H, Covarrubias S, Mak N, Agarwal A, Henkel R, et al. Effect of microsurgical varicocelectomy on fertility outcome and treatment plans of patients with severe oligozoospermia: an original report and meta-analysis. Andrologia. 2021;53:e14059. - PubMed
  56.  
    1. Enatsu N, Yamaguchi K, Chiba K, Miyake H, Fujisawa M. Clinical outcome of microsurgical varicocelectomy in infertile men with severe oligozoospermia. Urology. 2014;83:1071–1074. - PubMed
  57.  
    1. Dada R, Kumar R, Shamsi MB, Sidhu T, Mitra A, Singh S, et al. Azoospermia factor deletions in varicocele cases with severe oligozoospermia. Indian J Med Sci. 2007;61:505–510. - PubMed
  58.  
    1. Samplaski MK, Jarvi KA. Prognostic factors for a favorable outcome after varicocele repair in adolescents and adults. Asian J Androl. 2016;18:217–221. - PMC - PubMed
  59.  
    1. Samplaski MK, Yu C, Kattan MW, Lo KC, Grober ED, Zini A, et al. Nomograms for predicting changes in semen parameters in infertile men after varicocele repair. Fertil Steril. 2014;102:68–74. - PubMed
  60.  
    1. Kamal KM, Jarvi K, Zini A. Microsurgical varicocelectomy in the era of assisted reproductive technology: influence of initial semen quality on pregnancy rates. Fertil Steril. 2001;75:1013–1016. - PubMed
  61.  
    1. Ding H, Tian J, Du W, Zhang L, Wang H, Wang Z. Open non-microsurgical, laparoscopic or open microsurgical varicocelectomy for male infertility: a meta-analysis of randomized controlled trials. BJU Int. 2012;110:1536–1542. - PubMed
  62.  
    1. Lundy SD, Sabanegh ES., Jr Varicocele management for infertility and pain: a systematic review. Arab J Urol. 2017;16:157–170. - PMC - PubMed
  63.  
    1. Cocuzza M, Pagani R, Coelho R, Srougi M, Hallak J. The systematic use of intraoperative vascular Doppler ultrasound during microsurgical subinguinal varicocelectomy improves precise identification and preservation of testicular blood supply. Fertil Steril. 2010;93:2396–2399. - PubMed
  64.  
    1. Mehta A, Goldstein M. Microsurgical varicocelectomy: a review. Asian J Androl. 2013;15:56–60. - PMC - PubMed
  65.  
    1. Wang J, Xia SJ, Liu ZH, Tao L, Ge JF, Xu CM, et al. Inguinal and subinguinal micro-varicocelectomy, the optimal surgical management of varicocele: a meta-analysis. Asian J Androl. 2015;17:74–80. - PMC - PubMed
  66.  
    1. Colpi GM, Carmignani L, Nerva F, Piediferro G, Castiglioni F, Grugnetti C, et al. Surgical treatment of varicocele by a subinguinal approach combined with antegrade intraoperative sclerotherapy of venous vessels. BJU Int. 2006;97:142–145. - PubMed
  67.  
    1. Cassidy D, Jarvi K, Grober E, Lo K. Varicocele surgery or embolization: which is better? Can Urol Assoc J. 2012;6:266–268. - PMC - PubMed
  68.  
    1. Sayfan J, Adam YG, Soffer Y. A new entity in varicocele subfertility: the "cremasteric reflux". Fertil Steril. 1980;33:88–90. - PubMed
  69.  
    1. Goldstein M, Gilbert BR, Dicker AP, Dwosh J, Gnecco C. Microsurgical inguinal varicocelectomy with delivery of the testis: an artery and lymphatic sparing technique. J Urol. 1992;148:1808–1811. - PubMed
  70.  
    1. Ramasamy R, Schlegel PN. Microsurgical inguinal varicocelectomy with and without testicular delivery. Urology. 2006;68:1323–1326. - PubMed
  71.  
    1. Hou Y, Zhang Y, Zhang Y, Huo W, Li H. Comparison between microsurgical subinguinal varicocelectomy with and without testicular delivery for infertile men: is testicular delivery an unnecessary procedure. Urol J. 2015;12:2261–2266. - PubMed
  72.  
    1. Allameh F, Hasanzadeh Haddad A, Abedi A, Ranjbar A, Qashqai H, Fadavi B, et al. Varicocelectomy with primary gubernaculum veins closure: a randomised clinical trial. Andrologia. 2018 doi: 10.1111/and.12991. [Epub] - DOI - PubMed
  73.  
    1. Ou N, Zhu J, Zhang W, Liang Z, Hu R, Song Y, et al. Bilateral is superior to unilateral varicocelectomy in infertile men with bilateral varicocele: systematic review and meta-analysis. Andrologia. 2019;51:e13462. - PubMed
  74.  
    1. Niu Y, Wang D, Chen Y, Pokhrel G, Xu H, Wang T, et al. Comparison of clinical outcome of bilateral and unilateral varicocelectomy in infertile males with left clinical and right subclinical varicocele: a meta-analysis of randomised controlled trials. Andrologia. 2018;50:e13078. - PubMed
  75.  
    1. Sun XL, Wang JL, Peng YP, Gao QQ, Song T, Yu W, et al. Bilateral is superior to unilateral varicocelectomy in infertile males with left clinical and right subclinical varicocele: a prospective randomized controlled study. Int Urol Nephrol. 2018;50:205–210. - PubMed
  76.  
    1. Zheng YQ, Gao X, Li ZJ, Yu YL, Zhang ZG, Li W. Efficacy of bilateral and left varicocelectomy in infertile men with left clinical and right subclinical varicoceles: a comparative study. Urology. 2009;73:1236–1240. - PubMed
  77.  
    1. Chehval MJ, Purcell MH. Deterioration of semen parameters over time in men with untreated varicocele: evidence of progressive testicular damage. Fertil Steril. 1992;57:174–177. - PubMed
  78.  
    1. Addar AM, Nazer A, Almardawi A, Al Hathal N, Kattan S. The yield of microscopic varicocelectomy in men with severe oligospermia. Urol Ann. 2021;13:268–271. - PMC - PubMed
  79.  
    1. Chan PT, Wright EJ, Goldstein M. Incidence and postoperative outcomes of accidental ligation of the testicular artery during microsurgical varicocelectomy. J Urol. 2005;173:482–484. - PubMed
  80.  
    1. Barazani Y, Nagler HM. Other work has highlighted the limitations of using histopathology to predict success after varicocelectomy. Fertil Steril. 2011;95:487. - PubMed
  81.  
    1. Lund L, Roebuck DJ, Lee KH, Sørensen HT, Yeung CK. Clinical assessment after varicocelectomy. Scand J Urol Nephrol. 2000;34:119–122. - PubMed
  82.  
    1. Akcar Değirmenci N, Turgut M, Ozkan R. [Recurrence rate after varicocelectomy in infertile men] Tani Girisim Radyol. 2004;10:144–146. Turkish. - PubMed
  83.  
    1. Rotker K, Sigman M. Recurrent varicocele. Asian J Androl. 2016;18:229–233. - PMC - PubMed
  84.  
    1. Cayan S, Shavakhabov S, Kadioğlu A. Treatment of palpable varicocele in infertile men: a meta-analysis to define the best technique. J Androl. 2009;30:33–40. - PubMed
  85.  
    1. Franco G, Iori F, de Dominicis C, Dal Forno S, Mander A, Laurenti C. Challenging the role of cremasteric reflux in the pathogenesis of varicocele using a new venographic approach. J Urol. 1999;161:117–121. - PubMed
  86.  
    1. Kim KH, Lee JY, Kang DH, Lee H, Seo JT, Cho KS. Impact of surgical varicocele repair on pregnancy rate in subfertile men with clinical varicocele and impaired semen quality: a meta-analysis of randomized clinical trials. Korean J Urol. 2013;54:703–709. - PMC - PubMed
  87.  
    1. Baazeem A, Belzile E, Ciampi A, Dohle G, Jarvi K, Salonia A, et al. Varicocele and male factor infertility treatment: a new meta-analysis and review of the role of varicocele repair. Eur Urol. 2011;60:796–808. - PubMed
  88.  
    1. Fukuda T, Miyake H, Enatsu N, Matsushita K, Fujisawa M. Assessment of time-dependent changes in semen parameters in infertile men after microsurgical varicocelectomy. Urology. 2015;86:48–51. - PubMed
  89.  
    1. Al Bakri A, Lo K, Grober E, Cassidy D, Cardoso JP, Jarvi K. Time for improvement in semen parameters after varicocelectomy. J Urol. 2012;187:227–231. - PubMed
  90.  
    1. Ghaed MA, Makian SA, Moradi A, Maghsoudi R, Gandomi-Mohammadabadi A. Best time to wait for the improvement of the sperm parameter after varicocelectomy: 3 or 6 months. Arch Ital Urol Androl. 2020;92 doi: 10.4081/aiua.2020.3.259. - DOI - PubMed
  91.  
    1. Machen GL, Johnson D, Nissen MA, Naber E, Sandlow JI. Time to improvement of semen parameters after microscopic varicocelectomy: when it occurs and its effects on fertility. Andrologia. 2020;52:e13500. - PubMed
  92.  
    1. Masterson TA, Greer AB, Ramasamy R. Time to improvement in semen parameters after microsurgical varicocelectomy in men with severe oligospermia. Can Urol Assoc J. 2019;13:E66–E69. - PMC - PubMed
  93.  
    1. Seo JT, Kim KT, Moon MH, Kim WT. The significance of microsurgical varicocelectomy in the treatment of subclinical varicocele. Fertil Steril. 2010;93:1907–1910. - PubMed
  94.  
    1. Cantoro U, Polito M, Muzzonigro G. Reassessing the role of subclinical varicocele in infertile men with impaired semen quality: a prospective study. Urology. 2015;85:826–830. - PubMed
  95.  
    1. Elzanaty S. Varicocele repair in non-obstructive azoospermic men: diagnostic value of testicular biopsy - a meta-analysis. Scand J Urol. 2014;48:494–498. - PubMed
  96.  
    1. Weedin JW, Khera M, Lipshultz LI. Varicocele repair in patients with nonobstructive azoospermia: a meta-analysis. J Urol. 2010;183:2309–2315. - PubMed
  97.  
    1. Esteves SC, Miyaoka R, Roque M, Agarwal A. Outcome of varicocele repair in men with nonobstructive azoospermia: systematic review and meta-analysis. Asian J Androl. 2016;18:246–253. - PMC - PubMed
  98.  
    1. Berookhim BM, Schlegel PN. Azoospermia due to spermatogenic failure. Urol Clin North Am. 2014;41:97–113. - PubMed
  99.  
    1. Abdel-Meguid TA. Predictors of sperm recovery and azoospermia relapse in men with nonobstructive azoospermia after varicocele repair. J Urol. 2012;187:222–226. - PubMed
  100.  
    1. Lee JS, Park HJ, Seo JT. What is the indication of varicocelectomy in men with nonobstructive azoospermia? Urology. 2007;69:352–355. - PubMed
  101.  
    1. Sharma RK, Gupta S, Agarwal A, Finelli R, Kuroda S, Saleh R, et al. Role of cytocentrifugation combined with nuclear fast picroindigocarmine staining in detecting cryptozoospermia in men diagnosed with azoospermia. World J Mens Health. 2022 doi: 10.5534/wjmh.210210. [Epub] - DOI - PMC - PubMed
  102.  
    1. Krausz C, Riera-Escamilla A, Moreno-Mendoza D, Holleman K, Cioppi F, Algaba F, et al. Genetic dissection of spermatogenic arrest through exome analysis: clinical implications for the management of azoospermic men. Genet Med. 2020;22:1956–1966. - PMC - PubMed
  103.  
    1. Inci K, Hascicek M, Kara O, Dikmen AV, Gurgan T, Ergen A. Sperm retrieval and intracytoplasmic sperm injection in men with nonobstructive azoospermia, and treated and untreated varicocele. J Urol. 2009;182:1500–1505. - PubMed
  104.  
    1. Haydardedeoglu B, Turunc T, Kilicdag EB, Gul U, Bagis T. The effect of prior varicocelectomy in patients with nonobstructive azoospermia on intracytoplasmic sperm injection outcomes: a retrospective pilot study. Urology. 2010;75:83–86. - PubMed

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