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1P. Introduction

ale reproductive health has become an importantsue in current assisted reproduction. During

ecent years the perception of the male factorontributing to infertility has undergone a numberf revisions, realizing that >50% of infertility isntirely or in part due to a male factor [1]. Outcomesf assisted reproduction are primarily dependent one availability of viable sperm and age of the femaleember of the couple being treated. In azoospermicen intracytoplasmic sperm injection (ICSI) has

ecome the standard therapy [24]. Nevertheless,e treatment of obstructive and nonobstructive

zoospermia (NOA) will often include a surgicaltervention. For men with NOA, surgical sperm

etrieval is required to allow successful treatmentith ICSI. For men with obstructive azoospermia

sperm retrieval rates approach 100% and micro-surgical vasectomy reversal provides a very highchance of resulting in delivery of a child. Addition-ally, surgical treatment is more cost effective thanalternative forms of treatment such as assistedreproduction procedures alone [5,6]. The aim of thisarticle is to provide updated information regardingsurgical treatment options for male infertility and topresent current literature and data.

2. Testis biopsy

A testis biopsy is a diagnostic technique to assessspermatogenesis. It is most useful to determinewhether obstruction is the cause of azoospermia. Inmen with NOA testis biopsy can provide some, butnot absolute, diagnostic information. It can also rule

SIale infertilityESEesticular biopsyaricocele

sive treatments have been introduced. However, the management ofmale infertility will often involve surgical therapy, particularly withregard to azoospermia. For azoospermic men, surgical sperm retrievalis essential to allow subsequent treatment with assisted reproduction.Furthermore, a surgical approach allows diagnostic information to begathered regarding the cause and prognosis for treatment success.Surgical treatment of male infertility can be very successful at providinghigh rates of pregnancy and is typically more cost effective than alter-native forms of treatment such as assisted reproduction proceduresalone.

# 2007 European Association of Urology and European Board of Urology.

Published by Elsevier B.V. All rights reserved.

* Corresponding author. 525 East 68th Street, Starr 900, New York, NY 10021, USA.Tel. +1 212 746 5491; Fax: +1 212 746 8425.E-mail address: pnschleg@med.cornell.edu (P.N. Schlegel).

871-2592/$ see front matter# 2007 European Association of Urology and European Board of Urology. doi:10.1016/j.eeus.2007.02.001Surgery for Male Infertility

Peter N. Schlegel *, Markus Margreiter

Department of Urology, New York Presbyterian Hospital-Weill Medic

avai lab le at www.sciencedi rect .com

journa l homepage: www.europeanurology.com

Article info

Keywords:Azoospermia

Abstract

In the past decadublished by Elsevier B.V. All rights reserved.ollege of Cornell University, New York, NY, USA

there have been significant changes in the availableor infertile men. Novel medical and minimally inva-

Almost all men with the classic form (47,XXY) of

e au - e b u u p d a t e s e r i e s 5 ( 2 0 0 7 ) 1 0 5 1 1 2106out the unlikely possibility of testicular intratubulargerm cell neoplasia (carcinoma in situ) that is morecommon in men with unexplained unilateral testi-cular atrophy or with a history of cryptorchidism [7].Infertile men with abnormal semen analyses have a20-fold greater incidence of testicular cancer com-pared to the general population [8]. Furthermore, itis possible to take additional tissue during thisdiagnostic procedure that can be frozen for sub-sequent therapeutic trials of assisted reproduction.Cytologic evaluation, when performed concurrentlywith standard testicular biopsy, may provide impor-tant adjunctive information. Cytospin and touchprep techniques allow for the detection of latematuration arrest, which is not evaluable on fixedpermanent sections. Additionally, cytospin andtouch prep techniques allow the evaluation of thepresence of sperm within the seminiferous tubulewithout the removal of an additional piece oftesticular parenchyma. The wet prep techniqueallows the evaluation of sperm motility. The pre-sence of sperm motility appears to be highlyindicative of the presence of obstruction. Furtherinformation regarding the frequency of late matura-tion arrest and the endurance of the predictive valueof wet prep sperm motility is needed. At present,cytologic techniques should best be consideredadjuncts to, but not replacements of, carefulevaluation of fixed permanent testicular biopsyspecimens [9].

Adequate specimens for tissue evaluation can beobtained by open biopsy, needle biopsy, or, occa-sionally, fine-needle aspiration [1012]. Given thepotential inadequacy of needle biopsy or fine-needleaspiration, with the attendant risks to the vascu-lature of the testis, the open biopsy technique ispreferable [13,14]. The biopsy should be performedprior to reconstruction (rather than simultaneous tovasoepididymostomy), so that a definitive analysisof sperm production is possible on fixed sectionsprior to further exploration. Diagnostic informationon the status of spermatogenesis is most reliablydetermined on evaluation of a thin-sectioned,stained, fixed tissue specimen. In testicular biopsiesthe most advanced spermatogenic pattern, asopposed to the predominant pattern, appears toaffect the results of sperm retrieval. For men whohad at least one area of hypospermatogenesispresent on diagnostic testis biopsy, spermatozoawere retrieved in 57 of 73 attempts (81%), whereasfor men with maturation arrest as the mostadvanced pattern, spermatozoa were retrieved inonly 27 of 62 attempts (44%). If the entire diagnosticbiopsy had a Sertoli cell-only pattern, our most

recent data found that sperm could be retrieved forKlinefelters syndrome will be azoospermic, whereaslimited sperm production is commonly found in menwith a mosaic pattern of Klinefelters syndrome.Other karyotypic abnormalities identified includeRobertsonian translocations, chromosomal inver-sions, and sex chromosome abnormalities.

3.2. Y chromosome (AZF) microdeletions

Microdeletions on the long arm of the Y chromo-some have been demonstrated to disrupt sperma-togenesis in 515% of men with azoospermia orsevere oligospermia. Y chromosome microdeletionsaffecting fertility usually involve deletion of one or41% (98 of 257) of testicular sperm extraction (TESE)attempts [15]. Although no finding absolutelydetermined sperm retrieval or negated the possibi-lity of successful TESE, the findings of diagnosticbiopsy were helpful in evaluating the chance ofsuccess with testicular sperm extraction [16].

In the authors experience a diagnostic testisbiopsy is not required prior to TESE-ICSI for NOA. Adiagnostic biopsy should be performed if theetiology of azoospermia is not clear, if the risk ofcarcinoma in situ is high (rare), or if the results ofbiopsy will affect the couples choice to undergoTESE-ICSI [17].

3. Genetic abnormalities and testing

Genetic disorders are associated with spermato-genic failure. These abnormalities include chromo-somal abnormalities, detectable with routinekaryotype testing, Y chromosome microdeletions,so-called AZF defects and mutations in the cysticfibrosis transmembrane conductance regulator(CFTR) gene. It is apparent that assisted reproduc-tion and in particular ICSI may skew the naturalselection process and that a potential risk associatedwith its use is the transfer of genetic defects fromone generation to the next. Therefore, karyotypeevaluation and Y chromosome microdeletion ana-lysis is recommended for men with severe malefactor infertility, including sperm concentrations

with treatments that use the sperm of men with

e a u - e b u u p d a t e s e r i e s 5 ( 2 0 0 7 ) 1 0 5 1 1 2 107CBAVD [18].

4. Sperm retrieval for assisted reproduction

Sperm retrieval for use with the advanced form ofassisted reproduction, ICSI, is possible for manymen with obstructive azoospermia and NOA [19]. Inobstructive azoospermia, several techniques exist toallow for sperm retrieval rates approaching 100%. InNOA, TESE is essential for subsequent ICSI. How-ever, in patients with defective spermatogenesissperm retrieval is less certain [20]. Some couples willnot have sperm retrieved with TESE. Therefore, theuse of frozen donor spermatozoa as back-up shouldbe discussed prior to simultaneous TESE-ICSIattempts.

4.1. Obstructive azoospermia

It had long been thought that sperm exiting thetestis lack maturity, motility, and fertilizing cap-ability and that transit through the epididymis isessential to the acquisition of these features. In theunobstructed setting, sperm quality improves as thespermatozoa travel from caput to cauda; this is nottrue, however, in the obstructed setting. In repro-ductive tract obstruction, improved motility is seenspecific region that is missing on the Y chromosomemay provide prognostic significance. Approximatelytwo thirds of men with deletions involving onlyAZFc have sperm present in the ejaculate. Inazoospermic men with AZFc deletions, spermproduction is commonly present within the testicle,and TESE is as successful as for other men with NOA.For men with deletions involving the AZFb region,the chance of having sperm in the ejaculate orfinding sperm with TESE is severely decreased.Deletions involving the entire AZFa region are alsocommonly associated with a Sertoli cell-only pat-tern on diagnostic biopsy [17].

3.3. Cystic fibrosis gene mutation

A strong association exists between congenitalbilateral absence of the vas deferens (CBAVD) andmutations of the CFTR gene. About two thirds ofmen with CBAVD but no other clinical signs of cysticfibrosis have mutations of the CFTR gene. Therefore,it is important to test the partner for CFTR geneabnormalities before applying a treatment that useshis sperm. Genetic testing for CFTR mutations in thefemale partner should be offered before proceedingin sperm retrieved from the caput epididymiscompared to the cauda, as sperm extracted fromthe tail of an obstructed epididymis are in advancedstages of degeneration and necrosis. Thus, in thecase of obstruction, better quality sperm can befound proximally: in the rete testis, vasa efferentia,or caput epididymis; the more distal cauda epidi-dymis is the site of sperm degeneration. Thesefactors should be taken into account during anyattempt at sperm removal [9].

4.2. NOA

Human testicular histology is heterogeneous. Smallfoci of abnormal spermatogenesis can be adjacent tonormal seminiferous tubules. This formerly casualobservation is now the cornerstone of treatment formen with NOA. Successful sperm retrieval is possiblein most testicular sperm retrieval attempts in menwith NOA, despite diagnostic testis biopsy specimensshowing predominantly maturation arrest. Theability to retrieve sperm from the testes of men withNOA is independent of testicular size and follicle-stimulating hormone (FSH) level, but dependent onthe most advanced level of spermatogenesis identi-fied. All standard parameters of testicular evaluation(testicular volume, FSH, inhibin B levels) evaluateoverall function of the testis. Because sperm retrievaland pregnancy depend on finding sperm in just onesmall focus of the testis, the only predictor ofsuccessful treatment is the most developed regionof the testis, not thepredominant pattern of testicularhistology, overall testicular volume, or FSH level.These observations suggest that nearly all cases ofmale factor infertility can potentially be treated [9].

4.3. TESE

Scrotal exploration is performed through a medianraphe or transverse scrotal incision under local orgeneral anesthesia. Sperm are retrieved using anopen testicular biopsy technique. To confirm accu-rate identification of the testis and to avoid anyinjury to the epididymis, delivery of the testis isroutinely performed. Testicular blood vessels in thetunica albuginea are identified. An avascular regionnear the midportion of the medial, lateral, oranterior surface of the testis is chosen, and agenerous incision in the tunica albuginea, avoidingany capsular testicular vessels, is created to directlyexamine a wide area of testicular parenchyma.

4.4. Microdissection TESE

The technique that we developed allows the

removal of tiny volumes (23 mg) of testicular tissue

previously undergone multiple random biopsy TESE

e au - e b u u p d a t e s e r i e s 5 ( 2 0 0 7 ) 1 0 5 1 1 2108with improved sperm yield [21]. This techniquerequires use of an operating microscope and there isa brief learning curve to identify which tubulescontain spermatogenesis. The tubules containingsperm can often be visually identified under anoperating microscope after opening the testis, when1525 magnification is used to assist the biopsies.This approach (1) improves the yield of spermatozoaper biopsy, (2) results in less tissue removal, (3)makes the embryologists job easier in findingsperm because less tissue has to be examined,and (4) allows identification of blood vessels withinthe testicle, minimizing the risk of vascular injuryand loss of other areas of the testis [22,23]. Ourobservations of better sperm yield when usingmicrodissection TESE (vs. multiple random biopsies)has been confirmed by several other investigators[2426]. The benefit of microdissection TESE overstandard testis biopsies has been demonstrated inmultiple controlled surgical series. Amer et alcompared microdissection TESE with open surgicalbiopsy in the same patient. In this randomized,controlled trial the microsurgical approach wasfound to be relatively safer than the conventionaltechnique with significantly improved sperm yield[24]. Also Okada et al demonstrated a higher spermrecovery rate combined with a significantly lowercomplication rate for microdissection than forconventional TESE [25].

Encouraging experience has been obtained atWeill-Cornell with TESE-ICSI in the past 684attempted treatment cycles for couples in whomthe man had NOA. The mean age of patientsentering treatment was 36.1 yr for men and 32.1 yrfor women. In men, the initial mean serum FSHlevel was 22.7 IU/l (normal, 18 IU/l), and averagetestis volume 9.6 cc. During the past 684 attemptedTESE-ICSI cycles, sperm were retrieved for injec-tion in 406 cycles (59% retrieval rate). For thosecycles in which sperm were retrieved, the fertiliza-tion rate per injected oocyte was 59% (2299 of 4136),and embryo transfer occurred in 92% of cycles.Clinical pregnancies (fetal heartbeat on ultra-sound) were established in 48% (194 of 406) ofevaluable cycles and live deliveries occurred in 42%of cycles for which sufficient time had passedfor completed gestation. A total of 228 childrenhave been born from our center. Twin deliveriesoccurred in 11% of cases, triplets in

e a u - e b u u p d a t e s e r i e s 5 ( 2 0 0 7 ) 1 0 5 1 1 2 109compared the different treatment options forvaricocele. Cayan et al prospectively evaluated thedifference in sperm parameters, pregnancy andrecurrence rates, and complications after highligation surgery versus microsurgical high inguinalvaricocelectomy. His results showed significantlylower recurrence and hydrocele rates, a higherincrease in sperm motility, and higher pregnancyrates in patients undergoing a microsurgical var-icocelectomy [31]. Zucchi et al analyzed the outcomefollowing conventional open surgery with inguinalapproach versus antegrade sclerotherapy. Hedemonstrated that sclerotherapy combines shortersurgical time and faster recovery with comparableother parameters [32]. No prospective randomizedstudy comparing outcome and complications ofmicrosurgical approach with antegrade or retro-grade sclerotherapy exits.

Varicocelectomy involves ligation of all internalspermatic veins to prevent the retrograde flow ofblood in this system that is pathognomonic of avaricocele. To effectively and safely correct avaricocele, one should: (1) leave the vas deferensand its associated vessels intact, (2) divide allinternal spermatic veins (and external spermaticveins if the inguinal approach is used), and (3) leavethe lymphatic vessels and testicular arteries intact.Difficulty in visualizing any small internal spermaticvessels in the retroperitoneum explains the 10%clinical recurrence/persistence rate after a Palomovaricocelectomy. Even with a muscle-splittingapproach, more morbidity occurs with thisapproach than an inguinal approach.

The optimal surgical approach to varicocelec-tomy is an inguinal or subinguinal one, with at least68 optical magnification. If it is readily available,an operating microscope provides the ability to usevariable magnification during the procedure. In theauthors experience with both approaches, the useof an operating microscope clearly provides bettervisualization of the lymphatics and the testiculararteries during varicocelectomy. Although it istedious to perform a microsurgical dissection, theadvantages are that significant: testicular arteriescan be identified and preserved in >99.5% of cases,the varicocele recurrence/persistence rate is

was microsurgical vasectomy reversal. This treat-

7. Summary

e au - e b u u p d a t e s e r i e s 5 ( 2 0 0 7 ) 1 0 5 1 1 21106. Vasectomy reversal

Reversal of vasectomy is technically possible andhighly successful for a majority of men. The moderntechniques for vasovasostomy are modifications ofthe microsurgical approaches described in the mid-1970s by Drs. Owens and Silber. Microsurgicaltechniques generally have high postoperativepatency rates in experienced hands. Yet, only 5070% of couples actually achieve a pregnancy aftervasovasostomy [35]. The duration of time aftervasectomy is important. Secondary obstruction ofthe epididymis becomes increasingly more commonwhen>10 yr have passed after vasectomy. Althoughthe duration of time after vasectomy has an impacton pregnancy rate, Silber and Grotjan suggested thatthe age of the female partner has the greatestimpact. A review of 4010 cases performed by thesame surgeon showed that among female partnersunder age 30 yr at the time of vasectomy reversal,94.2% established a pregnancy, whereas only 61.1%of female partners aged 40 yr became pregnant.Regarding antisperm antibodies there is no clearevidence that they account for failure to conceiveafter vasectomy reversal [36]. Rather, it is likely thatfemale infertility, secondary obstruction in theepididymis, or recurrent obstruction at the anasto-motic site contribute to the inability to achievepregnancies in partners of men with establishedpatency after vasovasostomy.

The technique for vasectomy reversal (ie, vaso-vasostomy vs. vasoepididymostomy) depends onthe intravasal findings at the time of surgicalexploration. In addition, obstructive lesions mayoccur in the vas deferens at the inguinal level afterhernia repair. Testis biopsy is not routinely indi-cated prior to vasectomy reversal. Optimal resultswith vasovasostomy (or vasoepididymostomy) areachieved when these principles are followed: (1)accurate mucosa-to-mucosa anastomosis to allow aleakproof anastomosis, (2) tension-free anastomo-sis, (3) adequate blood supply to the ends of the vaswith healthy mucosa and muscularis, and (4)atraumatic technique. Adherence to these funda-mental principles is far more important than thenumber of layers performed or the exact suturematerial used.

Using a microsurgical approach, sperm appear inthe semen of 8590% of men, and 5070% of theirwives become pregnant after vasovasostomy [35].The Vasovasostomy Study Group found that resultswere progressively less favorable after microsurgicalvasectomy reversal as the obstructive interval (timefrom vasectomy until its reversal) lengthened [37].

That group reported rates of return of sperm to theSurgical treatment can be an effective approach forthe diagnosis and treatment of male infertility,particularly in men with obstructive azoospermia orNOA. Accurate identification of the cause of inferti-lity and microsurgical approaches to its manage-ment will often provide more effective treatmentwith lower morbidity. Appropriate training inmicrosurgery and overall experience with surgicaltechniques will produce the most effective treat-ment of the infertile man.

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CME questions

Please visit www.eu-acme.org/europeanurologyto answer these CME questions on-line. The CMEcredits will then be attributed automatically.

1. In patients with obstructive azoospermiaA. Nonmotile sperm can be found in the vasa

efferentia or caput epididymis.B. Sperm cannot be found in the vasa efferentia

or caput epididymis.C. Sperm quality improves as the spermatozoa

travel from caput to cauda.D. Sperm quality declines as the spermatozoa

travel from caput to cauda.

2. In testicular biopsiesA. The results provide definitive proof of whether

sperm will be found with testicular spermextraction.

3.

4. To effectively and safely correct a varicocele, oneshouldA. Leave the internal spermatic veins intact.B. Leave the external spermatic veins intact if the

inguinal approach is used.C. Divide the lymphatic vessels and leave the

testicular arteries intact.D. Leave the vas deferens and its associated

vessels intact.

5. Which appears to be the least important principlein achieving optimal results with vasovasos-tomy?A. Accurate mucosa-to-mucosa anastomosis to

allow a leak-proof anastomosis.B. Tension-free anastomosis.C. Adequate blood supply to the ends of the vas

with healthy mucosa and muscularis.D. Number of layers performed.

6. Using a microsurgical approach for vasovasost-

e au - e b u u p d a t e s e r i e s 5 ( 2 0 0 7 ) 1 0 5 1 1 2112Varicoceles occur inA. 15% of men with primary infertility.B. 35% of men with primary infertility.C. 53% of men with primary infertility.D. 81% of men with primary infertility.C. The most advanced spermatogenic patternappears to affect the results of sperm retrieval.

D. A Sertoli cell-only pattern negates the possibi-lity of successful testicular sperm extraction.results of sperm retrieval.

B. The predominant pattern appears to affect theA. Sperm appear in the semen of 8590% ofmen, and 7080% of their wives becomepregnant.

B. Sperm appear in the semen of 5060% ofmen, and 3040% of their wives becomepregnant.

C. Sperm appear in the semen of 6570% of men,and 4050% of their wives become pregnant.

D. Sperm appear in the semen of 8590% of men,and 5070% of their wives become pregnant.y,om

Surgery for Male InfertilityIntroductionTestis biopsyGenetic abnormalities and testingKaryotype evaluationY chromosome (AZF) microdeletionsCystic fibrosis gene mutation

Sperm retrieval for assisted reproductionObstructive azoospermiaNOATESEMicrodissection TESE

VaricocelectomyVasectomy reversalSummaryReferencesCME questions