Improvement of semen parameters after coil embolization of varicoceles: a systematic review

Melhora dos parâmetros seminais após embolização com molas de varicocele: uma revisão sistemática

Sergio Quilici Belczak Vanessa Stefaniak Leonardo Garcia Góes Felipe Coelho Neto Walter Jr. Boim de Araújo Nathalia Almeida Cardoso da Silva About the authors

Abstract

This systematic review was conducted in accordance with the 2009 Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement, including clinical studies in which one of the outcomes was semen parameter improvement after varicocele embolization using coils only. The objective of the review was to assess the evidence on the role of embolization using coils alone for semen parameter improvement in men with varicocele, since embolization using coils is the most cost-effective method of varicocele repair. Study quality was assessed using the methodological index for non-randomized studies (MINORS). Out of six retrospective and two prospective observational or comparative clinical studies involving 701 patients, semen concentration improved significantly in all five studies that assessed this parameter. Mean semen motility improved significantly in seven studies. The impact of embolization on semen density could not be analyzed.

Keywords:
varicocele; embolization with coils; semen parameters

Resumo

Trata-se de uma revisão sistemática conduzida de acordo com o PRISMA 2009 (Principais Itens para Relatar Revisões Sistemáticas e Metanálises) que incluiu estudos em que a melhora dos parâmetros seminais tenha sido um dos desfechos. Esta revisão foi realizada com o objetivo de avaliar as evidências sobre o papel da embolização com uso apenas de molas na melhora de parâmetros seminais em homens com varicocele, uma vez que a embolização apenas com molas é o método com melhor custo-benefício para o reparo de varicoceles. A qualidade dos estudos foi analisada com o índice MINORS. Em seis estudos clínicos retrospectivos e em outros dois prospectivos observacionais ou comparativos, a concentração seminal melhorou significativamente em todos os cinco estudos que avaliaram esse parâmetro. A motilidade seminal melhorou significativamente em sete estudos. Não foi possível analisar o impacto da embolização com molas na densidade seminal.

Palavras-chave:
varicocele; embolização com molas; parâmetros seminais

INTRODUCTION

Varicocele affects 15-22% of the male general population and can be present in 40% of men with abnormal semen analysis findings.11 Wagner L, Tostain J. Varicocèle et infertilité masculine: recommandations comité andrologie - AFU 2006. Prog Urol. 2007;17(1):12-7. http://dx.doi.org/10.1016/S1166-7087(07)92219-8. PMid:17373231.
http://dx.doi.org/10.1016/S1166-7087(07)...
The incidence of abnormal semen parameters can be as high as 40% in patients with varicocele and infertility, thus suggesting that varicocele may play an etiological role in relation to semen quality.22 World Health Organization – WHO.The influence of varicocele on parameters of fertility in a large group of men presenting to infertility clinics. Fertil Steril. 1992;57(6):1289-93. http://dx.doi.org/10.1016/S0015-0282(16)55089-4. PMid:1601152.
http://dx.doi.org/10.1016/S0015-0282(16)...
The first report correlating varicocele repair and improvement of semen parameters and fertility was published by Tulloch in 1955.33 Tulloch WS. Varicocele in subfertility; results of treatment. BMJ. 1955;2(4935):356-8. http://dx.doi.org/10.1136/bmj.2.4935.356. PMid:13240102.
http://dx.doi.org/10.1136/bmj.2.4935.356...
In fact, the main objective of varicocele repair is to reverse abnormal semen parameters, while effective improvement in pregnancy rates is still questionable.44 Baazeem A, Belzile E, Ciampi 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(4):796-808. http://dx.doi.org/10.1016/j.eururo.2011.06.018. PMid:21733620.
http://dx.doi.org/10.1016/j.eururo.2011....

The impact of varicocele repair on semen quality parameters has been much debated, since there are divergences in research results. Many studies, including important meta-analyses and their updates, have focused on assessing pregnancy rates, without considering the effect of varicocele repair on semen parameters and without including samples from men both with normal semen parameters and with subclinical varicoceles.55 Evers JL, Collins JA, Vandekerckhove P. Surgery or embolisation for varicocele in subfertile men. Cochrane Database Syst Rev. 2001;(1):CD000479. http://dx.doi.org/10.1002/14651858.CD000479. PMid:11279693.
http://dx.doi.org/10.1002/14651858.CD000...

6 Evers JL, Collins JA, Clarke J. Surgery or embolisation for varicocele in subfertile men. Cochrane Database Syst Rev. 2004;(3):CD000479. http://dx.doi.org/10.1002/14651858.CD000479.pub2. PMid:15266431.
http://dx.doi.org/10.1002/14651858.CD000...
-77 Evers JHLH, Collins J, Clarke J. Surgery or embolization of varicoceles in subfertile men. Cochrane Database Syst Rev. 2009;(1):CD000479. http://dx.doi.org/10.1002/14651858.CD000479.pub4. PMid:19160180.
http://dx.doi.org/10.1002/14651858.CD000...
These studies concluded that there was insufficient evidence to support the hypothesis that varicocele repair (surgery or embolization) could improve pregnancy rates among the partners of subfertile men.

On the other hand, a meta-analysis including two RCTs and three observational studies found that the odds of achieving spontaneous pregnancy from infertile men with clinical varicocele were significantly higher among those who underwent varicocele repair, compared with those who did not receive any treatment or received drug treatment.88 Marmar JL, Agarwal A, Prabakaran S, et al. Reassessing the value of varicocelectomy as a treatment for male subfertility with a new meta-analysis. Fertil Steril. 2007;88(3):639-48. http://dx.doi.org/10.1016/j.fertnstert.2006.12.008. PMid:17434508.
http://dx.doi.org/10.1016/j.fertnstert.2...
In another meta-analysis, focusing on the effect of clinical varicocele repair on the semen parameters of men with abnormal preoperative analysis findings, it was suggested that surgical varicocele repair may result in significant improvement in sperm concentration, motility, and morphology.99 Weidner W, Diemer T. Re: Reassessing the value of varicocelectomy as a treatment for male subfertility with a new meta-analysis. Eur Urol. 2008;54(2):465-6. http://dx.doi.org/10.1016/j.eururo.2008.04.090. PMid:19209437.
http://dx.doi.org/10.1016/j.eururo.2008....
Furthermore, Baazeem et al.44 Baazeem A, Belzile E, Ciampi 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(4):796-808. http://dx.doi.org/10.1016/j.eururo.2011.06.018. PMid:21733620.
http://dx.doi.org/10.1016/j.eururo.2011....
analyzed 22 prospective studies reporting on sperm concentration, 17 studies reporting on total semen motility, and five studies reporting on progressive motility before and after clinical varicocele repair and concluded that varicocelectomy was associated with significant increases in semen concentration and in total and progressive motility.

Since percutaneous embolization was first described by Lima et al.1010 Lima SS, Castro MP, Costa OF. A new method for the treatment of varicocele. Andrologia. 1978;10(2):103-6. http://dx.doi.org/10.1111/j.1439-0272.1978.tb01324.x. PMid:646140.
http://dx.doi.org/10.1111/j.1439-0272.19...
in 1978,the technique has been considered the least invasive approach for varicocele repair. Since that time, several studies have proven its efficacy for improving patients’ discomfort due to pain and also for improving sperm counts and even pregnancy outcomes. It also potentially has the advantages of less patient discomfort and faster recovery, compared with varicocelectomy.1111 Ali A, Wirth S, Treitl KM, Treitl M. Treatment of male varicoceles by transcatheter polidocanol foam sclerotherapy: evaluation of clinical success, complications, and patients’ satisfaction with regard to alternative techniques. Eur Radiol. 2015;25(10):2889-97. http://dx.doi.org/10.1007/s00330-015-3684-5. PMid:25796582.
http://dx.doi.org/10.1007/s00330-015-368...

12 Bechara CF, Weakley SM, Kougias P, et al. Percutaneous treatment of varicocele with microcoil embolization: comparison of treatment outcome with laparoscopic varicocelectomy. Vascular. 2009;17(Suppl. 3):S129-36. http://dx.doi.org/10.2310/6670.2009.00062. PMid:19919803.
http://dx.doi.org/10.2310/6670.2009.0006...
-1313 Gandini R, Konda D, Reale CA, et al. Male varicocele: transcatheter foam sclerotherapy with sodium tetradecyl sulfate--outcome in 244 patients. Radiology. 2008;246(2):612-8. http://dx.doi.org/10.1148/radiol.2462061295. PMid:18227549.
http://dx.doi.org/10.1148/radiol.2462061...
In a recent systematic review, varicocele embolization appeared to be safe and effective, irrespective of the embolic agent used (coils, sclerosants, or glues).1414 Makris GC, Efthymiou E, Little M, et al. Safety and effectiveness of the different types of embolic materials for the treatment of testicular varicoceles: a systematic review. Br J Radiol. 2018;91(1088):20170445. http://dx.doi.org/10.1259/bjr.20170445. PMid:29493263.
http://dx.doi.org/10.1259/bjr.20170445...
However, most studies focusing on semen parameters after varicocele embolization have included different embolic agents in the same investigation, without distinguishing between them.

The purpose of this study was to review the impact on semen parameters (semen density, concentration, and motility) of varicocele embolization specifically using coils.

MATERIALS AND METHODS

This systematic review was conducted in accordance with the 2009 PRISMA statement: Preferred Reporting Items for Systematic Reviews and Meta-Analysis.

Search of the literature

The literature was searched using the Medline, Embase, and Cochrane databases, looking for studies published in any language and at any time. The MeSH search headings “varicocele embolization”, “embolization with coil”, “sperm parameters”, and “fertility” were used in different combinations. The reference lists of the articles thus obtained (including systematic reviews) were carefully assessed for additional information. All abstracts were reviewed to make an initial selection of eligible studies. Two reviewers performed the search of the literature, study selection, data extraction, and quality evaluation. In any cases of disagreement, all other investigators evaluated the data to reach at a consensus. The search of the literature was concluded on January 31, 2019.

Study selection

The inclusion criteria that we defined for the analysis were that the studies should be clinical retrospective or prospective studies: (1) involving adult patients (at least 18 years old); (2) with testicular varicoceles (unilateral or bilateral); (3) who were treated with venous embolization using coils; and (4) reporting clinical semen parameter outcomes, specifically sperm concentration and motility.

Review articles, case reports, animal or in vitro studies, and editorials were excluded. Where multiple papers reported results from the same sample, the most recent one was included. All full articles that remained eligible after these exclusions were carefully reviewed.

Data extraction

Data were extracted from each study by two reviewers. The following information was gathered: authors and year of publication, study design, number of patients and their ages, inclusion criteria, varicocele side and grade, technical success, follow-up and outcomes, i.e. sperm density, concentration, and motility before and after varicocele embolization using coils.

Study quality assessment

The analysis of study quality was performed using the methodological index for non-randomized studies (MINORS).1515 Slim K, Nini E, Forestier D, Kwiatkowski F, Panis Y, Chipponi J. Methodological index for non-randomized studies (MINORS): development and validation of a new instrument. ANZ J Surg. 2003;73(9):712-6. http://dx.doi.org/10.1046/j.1445-2197.2003.02748.x. PMid:12956787.
http://dx.doi.org/10.1046/j.1445-2197.20...

Data analysis

Emphasis was placed on descriptive reports, due to the small number of studies and their reporting of outcomes associated with quite different endpoints.

RESULTS AND DISCUSSION

Following a rigorous study identification strategy (Figure 1), a total of eight studies1616 Prasivoravong J, Marcelli F, Lemaitre L, et al. Beneficial effects of varicocele embolization on semen parameters. Basic Clin Androl. 2014;24(1):9. http://dx.doi.org/10.1186/2051-4190-24-9. PMid:25780583.
http://dx.doi.org/10.1186/2051-4190-24-9...

17 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(4):826-30. http://dx.doi.org/10.1016/j.urology.2015.01.015. PMid:25817105.
http://dx.doi.org/10.1016/j.urology.2015...

18 Ferguson JM, Gillespie IN, Chalmers N, Elton RA, Hargreave TB. Percutaneous varicocele embolization in the treatment of infertility. Br J Radiol. 1995;68(811):700-3. http://dx.doi.org/10.1259/0007-1285-68-811-700. PMid:7640922.
http://dx.doi.org/10.1259/0007-1285-68-8...

19 Punekar SV, Prem AR, Ridhorkar HK, Deshmukh HL, Kelkar AR. Post-surgical recurrent varicocele: efficacy of internal spermatic venography and steel-coil embolization. Br J Urol. 1996;77(1):124-8. http://dx.doi.org/10.1046/j.1464-410X.1996.82321.x. PMid:8653282.
http://dx.doi.org/10.1046/j.1464-410X.19...

20 Shlansky-Goldberg RD, VanArsdalen KN, Rutter CM, et al. Percutaneous varicocele embolization versus surgical ligation for the treatment of infertility: changes in seminal parameters and pregnancy outcomes. J Vasc Interv Radiol. 1997;8(5):759-67. http://dx.doi.org/10.1016/S1051-0443(97)70657-2. PMid:9314365.
http://dx.doi.org/10.1016/S1051-0443(97)...

21 Tanahatoe SJ, Maas WM, Hompes PG, Lambalk CB. Influence of varicocele embolization on the choice of infertility treatment. Fertil Steril. 2004;81(6):1679-83. http://dx.doi.org/10.1016/j.fertnstert.2003.10.044. PMid:15193495.
http://dx.doi.org/10.1016/j.fertnstert.2...

22 Nabi G, Asterlings S, Greene DR, Marsh RL. Percutaneous embolization of varicoceles: outcomes and correlation of semen improvement with pregnancy. Urology. 2004;63(2):359-63. http://dx.doi.org/10.1016/j.urology.2003.09.026. PMid:14972491.
http://dx.doi.org/10.1016/j.urology.2003...
-2323 Binhazzaa M, Bounasr E, Perez G, et al. Comparaison de la cure de le varicocèle par ligature microchirurgicale subinguinale vs embolisation percutanée chez l’homme infertile. Prog Urol. 2016;26(16):1178-84. http://dx.doi.org/10.1016/j.purol.2016.09.064. PMid:27825582.
http://dx.doi.org/10.1016/j.purol.2016.0...
were included for analysis, comprising 701 patients who underwent varicocele embolization using coils (Table 1).

Figure 1
Study identification strategy.
Table 1
Characteristics of the studies on semen parameters after varicocele embolization using coils that were included in the present review.

There were two prospective studies1616 Prasivoravong J, Marcelli F, Lemaitre L, et al. Beneficial effects of varicocele embolization on semen parameters. Basic Clin Androl. 2014;24(1):9. http://dx.doi.org/10.1186/2051-4190-24-9. PMid:25780583.
http://dx.doi.org/10.1186/2051-4190-24-9...
,1717 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(4):826-30. http://dx.doi.org/10.1016/j.urology.2015.01.015. PMid:25817105.
http://dx.doi.org/10.1016/j.urology.2015...
and six retrospective studies.1818 Ferguson JM, Gillespie IN, Chalmers N, Elton RA, Hargreave TB. Percutaneous varicocele embolization in the treatment of infertility. Br J Radiol. 1995;68(811):700-3. http://dx.doi.org/10.1259/0007-1285-68-811-700. PMid:7640922.
http://dx.doi.org/10.1259/0007-1285-68-8...

19 Punekar SV, Prem AR, Ridhorkar HK, Deshmukh HL, Kelkar AR. Post-surgical recurrent varicocele: efficacy of internal spermatic venography and steel-coil embolization. Br J Urol. 1996;77(1):124-8. http://dx.doi.org/10.1046/j.1464-410X.1996.82321.x. PMid:8653282.
http://dx.doi.org/10.1046/j.1464-410X.19...

20 Shlansky-Goldberg RD, VanArsdalen KN, Rutter CM, et al. Percutaneous varicocele embolization versus surgical ligation for the treatment of infertility: changes in seminal parameters and pregnancy outcomes. J Vasc Interv Radiol. 1997;8(5):759-67. http://dx.doi.org/10.1016/S1051-0443(97)70657-2. PMid:9314365.
http://dx.doi.org/10.1016/S1051-0443(97)...

21 Tanahatoe SJ, Maas WM, Hompes PG, Lambalk CB. Influence of varicocele embolization on the choice of infertility treatment. Fertil Steril. 2004;81(6):1679-83. http://dx.doi.org/10.1016/j.fertnstert.2003.10.044. PMid:15193495.
http://dx.doi.org/10.1016/j.fertnstert.2...

22 Nabi G, Asterlings S, Greene DR, Marsh RL. Percutaneous embolization of varicoceles: outcomes and correlation of semen improvement with pregnancy. Urology. 2004;63(2):359-63. http://dx.doi.org/10.1016/j.urology.2003.09.026. PMid:14972491.
http://dx.doi.org/10.1016/j.urology.2003...
-2323 Binhazzaa M, Bounasr E, Perez G, et al. Comparaison de la cure de le varicocèle par ligature microchirurgicale subinguinale vs embolisation percutanée chez l’homme infertile. Prog Urol. 2016;26(16):1178-84. http://dx.doi.org/10.1016/j.purol.2016.09.064. PMid:27825582.
http://dx.doi.org/10.1016/j.purol.2016.0...
The length of follow-up ranged from 6 to 24 months. In most of the studies, the patients were declared to be older than 18 years, with mean ages ranging from 30.4 to 34 years. In three studies,1919 Punekar SV, Prem AR, Ridhorkar HK, Deshmukh HL, Kelkar AR. Post-surgical recurrent varicocele: efficacy of internal spermatic venography and steel-coil embolization. Br J Urol. 1996;77(1):124-8. http://dx.doi.org/10.1046/j.1464-410X.1996.82321.x. PMid:8653282.
http://dx.doi.org/10.1046/j.1464-410X.19...
,2222 Nabi G, Asterlings S, Greene DR, Marsh RL. Percutaneous embolization of varicoceles: outcomes and correlation of semen improvement with pregnancy. Urology. 2004;63(2):359-63. http://dx.doi.org/10.1016/j.urology.2003.09.026. PMid:14972491.
http://dx.doi.org/10.1016/j.urology.2003...
,2323 Binhazzaa M, Bounasr E, Perez G, et al. Comparaison de la cure de le varicocèle par ligature microchirurgicale subinguinale vs embolisation percutanée chez l’homme infertile. Prog Urol. 2016;26(16):1178-84. http://dx.doi.org/10.1016/j.purol.2016.09.064. PMid:27825582.
http://dx.doi.org/10.1016/j.purol.2016.0...
the patients’ ages were not reported, but it was clear that these subjects were adult males.

In all but one study,2121 Tanahatoe SJ, Maas WM, Hompes PG, Lambalk CB. Influence of varicocele embolization on the choice of infertility treatment. Fertil Steril. 2004;81(6):1679-83. http://dx.doi.org/10.1016/j.fertnstert.2003.10.044. PMid:15193495.
http://dx.doi.org/10.1016/j.fertnstert.2...
one of the inclusion criteria was presence of at least one abnormal semen parameter. In six studies, only primary clinical varicocele cases were included; one study1919 Punekar SV, Prem AR, Ridhorkar HK, Deshmukh HL, Kelkar AR. Post-surgical recurrent varicocele: efficacy of internal spermatic venography and steel-coil embolization. Br J Urol. 1996;77(1):124-8. http://dx.doi.org/10.1046/j.1464-410X.1996.82321.x. PMid:8653282.
http://dx.doi.org/10.1046/j.1464-410X.19...
related to recurrent varicoceles, and one other study1717 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(4):826-30. http://dx.doi.org/10.1016/j.urology.2015.01.015. PMid:25817105.
http://dx.doi.org/10.1016/j.urology.2015...
focused on subclinical varicoceles. In four studies, only left-side varicoceles were assessed. Varicocele grades were only reported in three studies1616 Prasivoravong J, Marcelli F, Lemaitre L, et al. Beneficial effects of varicocele embolization on semen parameters. Basic Clin Androl. 2014;24(1):9. http://dx.doi.org/10.1186/2051-4190-24-9. PMid:25780583.
http://dx.doi.org/10.1186/2051-4190-24-9...
,2121 Tanahatoe SJ, Maas WM, Hompes PG, Lambalk CB. Influence of varicocele embolization on the choice of infertility treatment. Fertil Steril. 2004;81(6):1679-83. http://dx.doi.org/10.1016/j.fertnstert.2003.10.044. PMid:15193495.
http://dx.doi.org/10.1016/j.fertnstert.2...
,2323 Binhazzaa M, Bounasr E, Perez G, et al. Comparaison de la cure de le varicocèle par ligature microchirurgicale subinguinale vs embolisation percutanée chez l’homme infertile. Prog Urol. 2016;26(16):1178-84. http://dx.doi.org/10.1016/j.purol.2016.09.064. PMid:27825582.
http://dx.doi.org/10.1016/j.purol.2016.0...
and, in one of these studies,1616 Prasivoravong J, Marcelli F, Lemaitre L, et al. Beneficial effects of varicocele embolization on semen parameters. Basic Clin Androl. 2014;24(1):9. http://dx.doi.org/10.1186/2051-4190-24-9. PMid:25780583.
http://dx.doi.org/10.1186/2051-4190-24-9...
grade III varicocele was an inclusion criterion.

The outcomes are presented in Table 2. The technical success rate of coil embolization was not reported in two studies,2121 Tanahatoe SJ, Maas WM, Hompes PG, Lambalk CB. Influence of varicocele embolization on the choice of infertility treatment. Fertil Steril. 2004;81(6):1679-83. http://dx.doi.org/10.1016/j.fertnstert.2003.10.044. PMid:15193495.
http://dx.doi.org/10.1016/j.fertnstert.2...
,2323 Binhazzaa M, Bounasr E, Perez G, et al. Comparaison de la cure de le varicocèle par ligature microchirurgicale subinguinale vs embolisation percutanée chez l’homme infertile. Prog Urol. 2016;26(16):1178-84. http://dx.doi.org/10.1016/j.purol.2016.09.064. PMid:27825582.
http://dx.doi.org/10.1016/j.purol.2016.0...
but it ranged from 85% to 100% (mean of 91.5%) in the six remaining studies.

Table 2
Outcomes from studies on semen parameters after varicocele embolization using coils.

Two studies1818 Ferguson JM, Gillespie IN, Chalmers N, Elton RA, Hargreave TB. Percutaneous varicocele embolization in the treatment of infertility. Br J Radiol. 1995;68(811):700-3. http://dx.doi.org/10.1259/0007-1285-68-811-700. PMid:7640922.
http://dx.doi.org/10.1259/0007-1285-68-8...
,2020 Shlansky-Goldberg RD, VanArsdalen KN, Rutter CM, et al. Percutaneous varicocele embolization versus surgical ligation for the treatment of infertility: changes in seminal parameters and pregnancy outcomes. J Vasc Interv Radiol. 1997;8(5):759-67. http://dx.doi.org/10.1016/S1051-0443(97)70657-2. PMid:9314365.
http://dx.doi.org/10.1016/S1051-0443(97)...
considered sperm density and motility as semen parameters; five studies focused on sperm concentration and motility; and one study2222 Nabi G, Asterlings S, Greene DR, Marsh RL. Percutaneous embolization of varicoceles: outcomes and correlation of semen improvement with pregnancy. Urology. 2004;63(2):359-63. http://dx.doi.org/10.1016/j.urology.2003.09.026. PMid:14972491.
http://dx.doi.org/10.1016/j.urology.2003...
only addressed motility. None of the studies included reported all three of these parameters together. All the studies reported the means for such parameters before and after varicocele embolization using coils (Table 2).

A significant improvement in density was reported in one study,2020 Shlansky-Goldberg RD, VanArsdalen KN, Rutter CM, et al. Percutaneous varicocele embolization versus surgical ligation for the treatment of infertility: changes in seminal parameters and pregnancy outcomes. J Vasc Interv Radiol. 1997;8(5):759-67. http://dx.doi.org/10.1016/S1051-0443(97)70657-2. PMid:9314365.
http://dx.doi.org/10.1016/S1051-0443(97)...
while another investigation1818 Ferguson JM, Gillespie IN, Chalmers N, Elton RA, Hargreave TB. Percutaneous varicocele embolization in the treatment of infertility. Br J Radiol. 1995;68(811):700-3. http://dx.doi.org/10.1259/0007-1285-68-811-700. PMid:7640922.
http://dx.doi.org/10.1259/0007-1285-68-8...
did not determine the difference in semen density from before to after embolization. Regarding semen concentration, all five studies that assessed this parameter reported significant improvement (mean before embolization: 10.8 x 106/ml; mean after embolization: 28.3 x 106/ml). The rates of semen concentration improvement ranged from 15% to as high as 550% (mean of 180%).

Semen motility was found to have improved significantly in seven studies, from a mean of 28.8% before embolization to a mean of 42.8% after varicocele repair (a mean improvement rate of 41.5%).

Only two studies also reported the percentages of patients presenting no improvement in the parameters studied after embolization. Although means for both parameters improved significantly in studies by Punekar et al.1919 Punekar SV, Prem AR, Ridhorkar HK, Deshmukh HL, Kelkar AR. Post-surgical recurrent varicocele: efficacy of internal spermatic venography and steel-coil embolization. Br J Urol. 1996;77(1):124-8. http://dx.doi.org/10.1046/j.1464-410X.1996.82321.x. PMid:8653282.
http://dx.doi.org/10.1046/j.1464-410X.19...
(semen concentration and motility) and Shlansky-Goldberg et al.2020 Shlansky-Goldberg RD, VanArsdalen KN, Rutter CM, et al. Percutaneous varicocele embolization versus surgical ligation for the treatment of infertility: changes in seminal parameters and pregnancy outcomes. J Vasc Interv Radiol. 1997;8(5):759-67. http://dx.doi.org/10.1016/S1051-0443(97)70657-2. PMid:9314365.
http://dx.doi.org/10.1016/S1051-0443(97)...
(semen density and motility), the former reported that 32.2% and the latter reported that 47.5% of their patients did not present any improvement in semen parameters after embolization.

The MINORS scores from the quality analysis of the studies included in this review ranged from 10 to 12 for the observational studies, considering 16 as the maximum score. MINORS scores for the comparative studies ranged from 18 to 20, considering 24 as the maximum score.

This systematic review focused on the impact on semen parameters of varicocele embolization using coils alone. A recent systematic review55 Evers JL, Collins JA, Vandekerckhove P. Surgery or embolisation for varicocele in subfertile men. Cochrane Database Syst Rev. 2001;(1):CD000479. http://dx.doi.org/10.1002/14651858.CD000479. PMid:11279693.
http://dx.doi.org/10.1002/14651858.CD000...
of the safety and effectiveness of different types of embolic materials (glues, coils, and sclerosants) for varicocele repair concluded that all of these materials are equally safe and effective, and that addition of sclerosants to embolization using coils did not appear to improve recurrence rates, although it obviously increased the cost and the length of the procedure. Although some systematic reviews55 Evers JL, Collins JA, Vandekerckhove P. Surgery or embolisation for varicocele in subfertile men. Cochrane Database Syst Rev. 2001;(1):CD000479. http://dx.doi.org/10.1002/14651858.CD000479. PMid:11279693.
http://dx.doi.org/10.1002/14651858.CD000...

6 Evers JL, Collins JA, Clarke J. Surgery or embolisation for varicocele in subfertile men. Cochrane Database Syst Rev. 2004;(3):CD000479. http://dx.doi.org/10.1002/14651858.CD000479.pub2. PMid:15266431.
http://dx.doi.org/10.1002/14651858.CD000...
-77 Evers JHLH, Collins J, Clarke J. Surgery or embolization of varicoceles in subfertile men. Cochrane Database Syst Rev. 2009;(1):CD000479. http://dx.doi.org/10.1002/14651858.CD000479.pub4. PMid:19160180.
http://dx.doi.org/10.1002/14651858.CD000...
have addressed the lack of evidence that varicocele repair improves semen parameters and/or pregnancy rates, it is well established that both varicocelectomy and varicocele embolization with different embolic materials are indeed associated with improvement in semen parameters.44 Baazeem A, Belzile E, Ciampi 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(4):796-808. http://dx.doi.org/10.1016/j.eururo.2011.06.018. PMid:21733620.
http://dx.doi.org/10.1016/j.eururo.2011....
,88 Marmar JL, Agarwal A, Prabakaran S, et al. Reassessing the value of varicocelectomy as a treatment for male subfertility with a new meta-analysis. Fertil Steril. 2007;88(3):639-48. http://dx.doi.org/10.1016/j.fertnstert.2006.12.008. PMid:17434508.
http://dx.doi.org/10.1016/j.fertnstert.2...
,99 Weidner W, Diemer T. Re: Reassessing the value of varicocelectomy as a treatment for male subfertility with a new meta-analysis. Eur Urol. 2008;54(2):465-6. http://dx.doi.org/10.1016/j.eururo.2008.04.090. PMid:19209437.
http://dx.doi.org/10.1016/j.eururo.2008....
,1111 Ali A, Wirth S, Treitl KM, Treitl M. Treatment of male varicoceles by transcatheter polidocanol foam sclerotherapy: evaluation of clinical success, complications, and patients’ satisfaction with regard to alternative techniques. Eur Radiol. 2015;25(10):2889-97. http://dx.doi.org/10.1007/s00330-015-3684-5. PMid:25796582.
http://dx.doi.org/10.1007/s00330-015-368...

12 Bechara CF, Weakley SM, Kougias P, et al. Percutaneous treatment of varicocele with microcoil embolization: comparison of treatment outcome with laparoscopic varicocelectomy. Vascular. 2009;17(Suppl. 3):S129-36. http://dx.doi.org/10.2310/6670.2009.00062. PMid:19919803.
http://dx.doi.org/10.2310/6670.2009.0006...

13 Gandini R, Konda D, Reale CA, et al. Male varicocele: transcatheter foam sclerotherapy with sodium tetradecyl sulfate--outcome in 244 patients. Radiology. 2008;246(2):612-8. http://dx.doi.org/10.1148/radiol.2462061295. PMid:18227549.
http://dx.doi.org/10.1148/radiol.2462061...
-1414 Makris GC, Efthymiou E, Little M, et al. Safety and effectiveness of the different types of embolic materials for the treatment of testicular varicoceles: a systematic review. Br J Radiol. 2018;91(1088):20170445. http://dx.doi.org/10.1259/bjr.20170445. PMid:29493263.
http://dx.doi.org/10.1259/bjr.20170445...
Since embolization using coils is undoubtedly the most cost-effective method for varicocele repair and improvement of semen parameters is the main objective of this treatment, it seemed important to review and assess the impact on these parameters of varicocele embolization using coils.

Regarding semen density, the present review did not compile evidence that could support any definitive conclusions. Whereas Ferguson et al.1818 Ferguson JM, Gillespie IN, Chalmers N, Elton RA, Hargreave TB. Percutaneous varicocele embolization in the treatment of infertility. Br J Radiol. 1995;68(811):700-3. http://dx.doi.org/10.1259/0007-1285-68-811-700. PMid:7640922.
http://dx.doi.org/10.1259/0007-1285-68-8...
reported that 24 months after repair there was only a trend towards improvement in semen density among 87 men with clinical left varicocele and abnormal semen parameters, Shlansky-Goldberg et al.2020 Shlansky-Goldberg RD, VanArsdalen KN, Rutter CM, et al. Percutaneous varicocele embolization versus surgical ligation for the treatment of infertility: changes in seminal parameters and pregnancy outcomes. J Vasc Interv Radiol. 1997;8(5):759-67. http://dx.doi.org/10.1016/S1051-0443(97)70657-2. PMid:9314365.
http://dx.doi.org/10.1016/S1051-0443(97)...
reported that a significant improvement in semen density was achieved in 173 patients with clinical left, right, and bilateral varicoceles and small varicoceles, which was confirmed via ultrasound after a follow-up period of unspecified length. Ferguson et al.1818 Ferguson JM, Gillespie IN, Chalmers N, Elton RA, Hargreave TB. Percutaneous varicocele embolization in the treatment of infertility. Br J Radiol. 1995;68(811):700-3. http://dx.doi.org/10.1259/0007-1285-68-811-700. PMid:7640922.
http://dx.doi.org/10.1259/0007-1285-68-8...
did not discuss their observed trend towards improvement in semen density in greater detail. However, Shlansky-Goldberg et al.2020 Shlansky-Goldberg RD, VanArsdalen KN, Rutter CM, et al. Percutaneous varicocele embolization versus surgical ligation for the treatment of infertility: changes in seminal parameters and pregnancy outcomes. J Vasc Interv Radiol. 1997;8(5):759-67. http://dx.doi.org/10.1016/S1051-0443(97)70657-2. PMid:9314365.
http://dx.doi.org/10.1016/S1051-0443(97)...
mentioned a critical review by Schlesinger et al.,2424 Schlesinger MH, Wilets IF, Nagler HM. Treatment outcome after varicocelectomy. a critical analysis. Urol Clin North Am. 1994;21(3):517-29. PMid:8059505. in which 12 out of 16 studies demonstrated significant improvements in semen density after varicocelectomy, along with a strong association between improvement in semen density and improvement in semen motility. Shlansky-Goldberg et al.2020 Shlansky-Goldberg RD, VanArsdalen KN, Rutter CM, et al. Percutaneous varicocele embolization versus surgical ligation for the treatment of infertility: changes in seminal parameters and pregnancy outcomes. J Vasc Interv Radiol. 1997;8(5):759-67. http://dx.doi.org/10.1016/S1051-0443(97)70657-2. PMid:9314365.
http://dx.doi.org/10.1016/S1051-0443(97)...
also found similar results regarding semen parameters through comparing varicocelectomy and embolization using coils for varicocele repair.

Semen concentration improved significantly after embolization using coils in all the studies reviewed here that assessed this parameter (100%), including patients both with recurrent varicoceles (n = 28) and with subclinical varicoceles (n = 218), while semen motility improved significantly in seven studies (87.5%).

Nabi et al.2222 Nabi G, Asterlings S, Greene DR, Marsh RL. Percutaneous embolization of varicoceles: outcomes and correlation of semen improvement with pregnancy. Urology. 2004;63(2):359-63. http://dx.doi.org/10.1016/j.urology.2003.09.026. PMid:14972491.
http://dx.doi.org/10.1016/j.urology.2003...
analyzed semen motility alone, in relation to morphology, among 71 patients with clinical varicocele. These patients were divided into four groups according to their semen density measured before embolization: ≤ 10 million/ml, 10-30 million/ml, 30-60 million/ml, and ≥ 60 million/ml. Six and twelve months after embolization, significant improvement in semen quality was observed only for the group with previous semen density of 10-30 million/ml, thus suggesting that motility improvement is density-dependent.

Tanahatoe et al.2121 Tanahatoe SJ, Maas WM, Hompes PG, Lambalk CB. Influence of varicocele embolization on the choice of infertility treatment. Fertil Steril. 2004;81(6):1679-83. http://dx.doi.org/10.1016/j.fertnstert.2003.10.044. PMid:15193495.
http://dx.doi.org/10.1016/j.fertnstert.2...
compared semen quality between patients who underwent embolization using coils and those who decided not to have their clinical varicocele treated. They observed that decreases in semen quality were significantly greater in the control group, which confirms the progressively deleterious effect of varicocele on sperm quality.2525 Cozzolino DJ, Lipshultz LI. Varicocele as a progressive lesion: positive effect of varicocele repair. Hum Reprod Update. 2001;7(1):55-8. http://dx.doi.org/10.1093/humupd/7.1.55. PMid:11212075.
http://dx.doi.org/10.1093/humupd/7.1.55...
The main purpose of that study2121 Tanahatoe SJ, Maas WM, Hompes PG, Lambalk CB. Influence of varicocele embolization on the choice of infertility treatment. Fertil Steril. 2004;81(6):1679-83. http://dx.doi.org/10.1016/j.fertnstert.2003.10.044. PMid:15193495.
http://dx.doi.org/10.1016/j.fertnstert.2...
was to investigate whether improvement of semen quality after embolization would enable use of less-invasive modes of assisted reproductive technology. The study confirmed this hypothesis.

The limitations of the present review include the fact that most of the studies on which this review was based were retrospective, with heterogeneous criteria for patient inclusion. Furthermore, neither the purely observation studies nor the comparative studies achieved the maximum MINORS score, although no poor scores were observed. Lastly, the differing endpoints chosen by authors, across only eight studies, made it difficult to perform statistical analysis of their results and may have influenced our descriptive analysis.

Nonetheless, it is clear that varicocele repair, whether using various open surgery techniques or by embolization using different embolic agents, is associated with significant improvement in sperm concentration and motility, despite the deficient evidence demonstrating a beneficial effect on spontaneous pregnancy rates.44 Baazeem A, Belzile E, Ciampi 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(4):796-808. http://dx.doi.org/10.1016/j.eururo.2011.06.018. PMid:21733620.
http://dx.doi.org/10.1016/j.eururo.2011....
The rate of pregnancies after varicocele repair was not included as an endpoint in this review; a further systematic review exclusively focused on this matter will be conducted.

In this review, embolization using coils alone was seen to play the same important role for improving semen parameters as other types of repair. In addition, embolization using coils alone presented advantages such as low cost, ambulatory management, local anesthesia only, and faster recovery.

CONCLUSION

Embolization using coils was associated with improvement in semen concentration and motility in cases of clinical, recurrent, or subclinical varicoceles. There was insufficient data to draw conclusions on the impact of these varicocele repairs on semen density.

  • How to cite: Belczak SQ, Stefaniak V, Góes LG, Coelho Neto F, Araújo WJB, Silva NAC. Improvement of semen parameters after coil embolization of varicoceles: a systematic review. J Vasc Bras. 2021;20:e20200137. https://doi.org/10.1590/1677-5449.200137
  • Financial support: None.
  • The study was carried out at Faculdade de Medicina, Centro Universitário São Camilo, São Paulo, SP, Brazil.

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Publication Dates

  • Publication in this collection
    28 Apr 2021
  • Date of issue
    2021

History

  • Received
    22 July 2020
  • Accepted
    31 Aug 2020
Sociedade Brasileira de Angiologia e de Cirurgia Vascular (SBACV) Rua Estela, 515, bloco E, conj. 21, Vila Mariana, CEP04011-002 - São Paulo, SP, Tel.: (11) 5084.3482 / 5084.2853 - Porto Alegre - RS - Brazil
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