REVIEW

Microdissection testicular sperm extraction for
non-obstructive azoospermia: The assessment of serum
hormone levels before and after procedure
Tomomoto ISHIKAWA１） and Masato FUJISAWA２）
Department of Anatomy and Developmental Biology, Monash University, Clayton, Victoria 3800, Australia
Division of Urology, Department of Surgery Related, Faculty of Medicine, Kobe University Graduate School of Medicine, Kobe,
650 -0017 Japan

１）

２）

Introduction

nadism and infertility. In all patients in whom microTESE was successful we could identify focal sperma-

Microdissection testicular sperm extraction （micro-

togenesis in dilated and opaque seminiferous tubules

TESE） has become a recognized procedure for men

surrounded by shrunken tubules or fibrous tissue.

with nonobstructive azoospermia （NOA）. Micro-TESE

Micro-TESE

and intracytoplasmic sperm injection（ICSI）cycles ex-

sperm retrieval in KS cases.

isparticularly

helpfulforsuccessful

pose the couple to an emotional and financial burden,

Although numerous studies have compared conven-so it would be beneficial to predict the success oftional versus micro-TESE ［２, ３, ５］, there are a few

sperm retrieval using noninvasive parameters before

large comprehensive study analyzing the hormonal

attempted procedure.

changes after micro-TESE. In addition, especially KS

It has been noted that micro-TESE done while ob-patients, the study of hormonal change after micro-

serving the seminiferous tubules under an operating

TESE is lacking. Hypogonadism in KS is relative

microscope could minimize the damage to testicularrather than absolute and has been found to be an in-tissue, while maximizing sperm recovery, compared todependent risk factor for development of abdominal

randomadiposity ［６］. Hypogonadism is also associated withbiopsies［１］. Micro-TESE

has

also

been

shown to be more successful in sperm retrieval thanmetabolic syndrome and type ２ diabetes［７］.

a single biopsy or multiple random biopsies［２, ３］. In

We reviewed the outcomes of micro-TESE, primar-

addition, micro-TESE improves the yield of spermato-

ily the sperm retrieval in patients with elevated serum

zoa per biopsy, results in less tissue removal （andFSH. We also analyzed the predictive value of gona-loss of testicle）, and allows identification of blood ves-

dotropin and biopsy histology for retrieving testicularsels within the testicle, minimizing the risk of vascu-

sperm by micro-TESE in NOA patients. In addition,

lar injury and loss of other areas of the testis ［１］.

we reviewed complications in this procedure for theThus, micro-TESE is based on the principle of identi-

patients between ４
６XY males with NOA and KS dur-fying the most advanced pattern, not necessarily theing follow-up.

predominant pattern, of spermatogenesis in the testis.
Although FSH reflects the predominant pattern of

Sperm retrieval techniquespermatogenesis, it may not reflect isolated areas ofspermatogenesis within the testis.

The sperm extraction procedures have been exten-

Klinefelter syndrome （KS） is the most common

sively described already. In cases of NOA, the proce-sex-chromosome disorder, with a prevalence of １ indure was often extensive, involving general anesthesia

６
６
０ men ［４］, and is a frequent cause of hypogo-and micro-TESE until sufficient spermatozoa were extracted for ICSI. Micro-TESE was used in which

Correspondence : Tomomoto ISHIKAWA, Department of
Anatomy and Developmental Biology, Monash University,
Clayton, Victoria ３
８００, Australia
TEL ：＋６
１―３―９
９
０
２
９
２
８
６
FAX：＋６
１―３―９
９
０
２
９
２
２
３
E-mail : Tomomoto.Ishikawa@med.monash.edu.au

seminiferous tubule are directly examined throughout
the testis using an operating microscope and selectively biopsied for all of the NOA patients as below
in Schlegel’s method. Briefly, a midline incision was

Japanese Journal of Reproductive Endocrinology（2009）14 : 15-20

15

Tomomoto ISHIKAWA et al.

Table1Comparison of SRR between conventional and micro-TESE
Case SRR by conventional SRR by micro-TESE（％）（n） TESE（％）

Year

Author

１
９
９
９
２
０
０
２
２
０
０
２
２
０
０
２
２
０
０
４
２
０
０
５
２
０
０
５
２
０
０
９
２
０
０
９

Schlegel et al.
Amer et al.
Okada et al.
Tsujimura et al.
Tsujimura et al.
Ramasamy et al.
Mulhall et al.
Ramasamy et al.
Ishikawa et al.

２
７
１
０
０
７
４
５
６
１
８
０
４
６
０
４
８
７
９
２
１
５
０

４
５
３
０
１
６．
７
３
５．
１
−
３
２
５
０
−
−

６
３
４
７
４
４．
６
４
２．
９
４
４．
４
５
８
４
５
６
０
４
２
（３
２，
４
４，
４
８）

TESE, testicular sperm extraction.

the results of ７
９
２ procedures achieving a SRR of
Fig．
１

６
０％［１
１］
. We reported the learning curves that SRR

made in the scrotum, and the tunica vaginalis waslatest ５０ cases （４８％） was significantly higher thanopened and the testis covered with the tunica albugi-

first ５０ cases（３２％）. SRR of micro-TESE are strongly

nea was visualized. The remainder of the procedure

influenced by the surgeon’s case volume. A consider-

was performed under an operative microscope. Afterable amount of cases is necessary to reach an opti-

the tunica albuginea was opened, direct examination

mal plateau level of SRR in this microscopic surgery

for NOA patients in the mid ５
０ cases（４４％）and theof the testicular parenchyma was performed at x１
５２
-５

［１
２］
. The outcome of SRR may depend on factors

magnification（Fig．１）. Small samples（５１- ０mg）wereother than surgical technique, such as embryologists’excised from the tubules. If no spermatozoa werelearning curves.

identified in the initial sample, subsequent samples
were taken from the same testis and, if needed, fromthecontralateral

testis.

Dissection

was

performed

Biopsy histology for SRR by micro-TESE in
NOA patients

through all regions of testicular tissue, preserving thetesticular blood supply. The procedure was terminatedPathological findings are important ; many reports

when spermatozoa were retrieved or when further

have shown a relation between successful TESE anddissection was thought likely to jeopardize the testicu-

５］. Tsujimura et al.［３］testicular histopathology［１３―１

lar blood supply［８］. In general, we define success ofreported that SRR by micro-TESE for patients with

sperm retrieval as the recovery of at least one sper-

Sertolimatozoa.

whereas that by conventional TESE was １
３％. Fur-

cell

only

syndrome （ SCO ） was２
２.５％ ,

thermore, SRR by micro-TESE for patients with hypo-

Sperm retrieval rate（SRR）by micro-TESE

spermatogenesis was １
００％, whereas that by conventional TESE was ７
６.９％. Okada et al. also reported

The outcome of micro-TESE has been reported

the reasonable result showing that SRR by micro-

２］. In １９
９
９, the first report on（Table １）［１―３, ５, ８―１

TESE for hypospermatogenesis was １
００％. They also

this technique compared ２
２ patients whom underwent

reported that SRRs by micro-TESE for maturation ar-standard multiple biopsy with a group of ２
７ men un-rest （MA） and SCO were ７
５％ and ３
３.９％, respec-

dergoing micro-TESE. The author describes a signifi-

tively, whereas those by conventional TESE werecant improvement on the SRR when micro-TESE had

３
７.５％ and ６.３％ ［２］. Ramasamy et al. ［８］ reported

been performed（６３ versus ４５％）［１］. A comparative

SRRs of ８１％, ４４％, and ４
１％ for hypospermatogene-study including １
１
６ men found a significantly higher

sis, MA, and SCO, respectively. We reported SRRs of

SRR with the addition of optical magnification com-２］
. Thus, it is
１
０
０％, ５
０％, and ２
７.８％, respectively［１pared with conventional TESE （４７ versus ３
０％）
［５］
.

well accepted that micro-TESE offers a great advan-

To date, the largest series on Micro-TESE reported

tage for patients with all types of testicular histology.

16

Japanese Journal of Reproductive Endocrinology Vol.14 2009

Micro-TESE for NOA and hormonal assay

genic function and histology of the testis as a whole.

Micro-TESE for KS

Therefore, FSH may predict the presence of sperm at
random biopsy using conventional TESE techniques

It has been reported that focal spermatogenesis can

５］. However, it is even more difficult to predict［２
２―２

result in ejaculated spermatozoa or the retrieval of

the presence of testicular spermatozoa in infertile men

spermatozoa by micro-TESE. Several studies havewith severely impaired spermatogenesis. Serum FSH

been conducted with micro-TESE in patients with KS

concentration is not related to the more advanced

８］. Schiffe et al. reported an impressive SRR［１
６―１

stages of spermatogenesis ［２６］. The relationship of（６９.０％）; however, these cases of KS were including

FSH with spermatogenesis is not straightforward inmosaic type［１７］. We reproted a SRR of ５
２.４％ of ２
１

men with NOA. Serum FSH level has a poor predic-

patients with non-mosaic KS by micro-TESE ［１２］. It

tive value for successful micro-TESE.

has been reported that patient age in successful

Hung et al. have recently reported a subset of men

TESE for cases of KS is significantly younger thanwith normal FSH, normalsized testes, and diffuse MA,that in failed cases ［１
６, １
９, ２
０］
. In NOA, the ab-

who had lower sperm retrieval rates［２７］. Therefore,

sence of uniformity in testicular tissue is a criticalin this subgroup of men with diffuse MA and normal

key to succeed and rationale in micro-TESE. If better

FSH, the FSH level may reflect adequate control feed-

portion or best portion can be identified under micro-back from germ cells and Sertoli cells despite the ab-scope, there is an increased chance to retrieve tes-

sence of sperm production. Ramasamy et al.［１１］ticular sperm. In men with KS, the histological diag-showed that sperm retrieval was higher in NOA men

nosis was uniformly the SCO syndrome. In all pa-

with FSH＞１
５ IU/mL than those men with FSH＜１
５tients in whom micro-TESE was successful we could

IU/mL. Also, sperm retrieval rates were maintained

identify focal spermatogenesis in dilated and opaqueeven when the FSH value was markedly elevated.

seminiferous tubules surrounded by shrunken tubules

Lower FSH may be a reflection of the larger number

or fibrous tissue. Micro-TESE is particularly helpfulof Sertoli cells in a larger testis, providing more con-for successful sperm retrieval in KS cases.

trol feedback to suppress FSH production. The excellent findings with higher FSH may reflect the sensi-

Predictors for sperm retrieval

tivity of microdissection in finding small areas ofsperm production. It further illustrates that FSH is

Recently, the most popular treatment in patients

not able to resolve spermatogenesis on an individualwith NOA has been micro-TESE with subsequent as-

tubule level, and, therefore, they should not be usedsisted fertilization by intracytoplasmic sperm injection

as predictors of sperm recovery.

（ICSI）. With the spread of ICSI, the presence of a

Recent reports have suggested that the serum con-minimum number of spermatozoa is required for fer-

centration of inhibin B may be a good non-invasive

tilization. Micro-TESE and intracytoplasmic sperm in-

１］
predictor of spermatozoa retrieval by TESE ［２８―３jection （ICSI） cycles expose the couple to an emo-

The production of sufficient inhibin B to maintain de-tional and financial burden, so it would be beneficial

tectable serum concentrations in adults depends on

to predict the success of sperm retrieval using nonin-

spermatogenic activity. Inhibin B has been found tovasive parameters before attempted procedure. An im-

be slightly more sensitive than FSH as an index of

portant preoperative serum parameter studied in the

spermatogenic status ［３２］. However, the predictive

first years of TESE was FSH. In general, the serum

value of inhibin B is not considered sufficient to ex-

concentration of FSH is inversely correlated with im-

clude or include patients for TESE ［３３, ３４］. There-pairment of spermatogenesis. Recent studies havefore, a prognostic parameter for successful sperm re-shown that elevated FSH levels have been associatedtrieval in TESE seems to be decisive for male fertil-with a low probability for the retrieval of spermatozoa

ity. It is important to provide predictive information to

in men ［２１］ using random biopsy TESE techniques.

patients and their spouses preoperatively and to allow

Serum FSH is an indirect reflection of the spermato-

them to determine whether to undergo micro-TESE.

REVIEW17

Tomomoto ISHIKAWA et al.

We conclude that at the present time there are nochange in FSH levels for ４
６XY males with NOA may

absolute predictors of sperm yield for micro-TESE.

have been a result of the scar tissue left behind in
the testis with local germ cell loss near the scar after

Postoperative complication

the procedure ［３９］. Tash et al. ［３９］ also suggested
an increase in peritubular scar tissue that may have

Although numerous studies have compared conven-affected Leydig cells as well as germ cell number.

tional versus micro-TESE ［２, ３, ５］, there are a few

The changes in FSH and LH after micro-TESE maylarge comprehensive study analyzing the hormonalsuggest that the testes of NOA patients overall may

changes after micro-TESE. In addition, especially KS

be better able to respond than KS patients. Thispatients, the study of hormonal change after micro-

could reflect １）a defect in pituitary responsiveness of
KS patients, or ２） better testicular response in idi-

TESE is lacking.
Given the testicular anatomic consideration, multiplesite testicular biopsy is suspected to increase the riskoftesticulardamagecausedbyinterruption

opathic NOA patients.
Even Micro-TESE could be suspected to increaseof

the risk of testicular damage caused by interruption

branches of the testicular artery［３５］or pressure at-of branches of the testicular artery, pressure atrophy

rophy from intratesticular swelling and hematoma

from intratesticular swelling, or an increase in peritu-

［３
６］
.

bular scar tissue that may have affected Leydig cells

The most important advantage of micro-TESE isas well as germ cell number. This technique was de-that meticulous hemostasis can be achieved underveloped to minimize unnecessary damage to the testis

clear magnified vision. Ramasamy et al. ［８］ reported

and also to improve the sperm recovery. T itself maythat for NOA patients, the initial decrease was fol-

have a central or permissive role in the pathogenesis

lowed by a return to ９
５％ of the pre-micro-TESE T

of the metabolic syndrome and type ２ diabetes by in-levels at the end of １
８ months. In KS but not ４
６XY

creasing skeletal muscle tissue and decreasing ab-males with NOA, a decrease in the serum T levels

dominal obesity and nonesterified fatty acids, conse-

after micro-TESE was noted. A recent study on micro-

quently improving insulin sensitivity ［４０］. Hypogo-

TESE for NOA also reported no change in T after

nadism in KS may cause an unfavorable change inthe procedure ［３７］. However, interestingly, our KS

body composition and metabolic syndrome ［４１］. We

study series demonstrated a significant decline in T

may recommend that patients in KS with low T level

by ３
０３- ５％ （P ＜０.０
１） at １ to １
２ months, and re-after micro-TESE may be treated properly to prevent

turned to ７
５％ of the pre-TESE levels after １
８

the long-term deleterious consequences of hypogo-months. The change in T levels in KS may havenadism. We would like to add that since serum T

been a result of the much smaller testis and Leydig

levels are abnormal at baseline for KS patients, incell loss near the scar after the procedure［３８］.

general, many KS patients（before micro-TESE）were

In addition, Ramasamy et al. ［８］ showed that for

already candidates for androgen replacement.

NOA patients the mean FSH levels increased after

Although the microdissection procedure is relatively

micro-TESE significantly, but no significant difference

safer and improves the sperm retrieval rate signifi-

in the LH levels was noted between the preoperative

cantly in patients with NOA, we should take care ofand postoperative groups. In our data, in ４
６XY males

the hypogonadism in KS patients after even microdis-

with NOA, serum levels of FSH increased significantly

section procedure.

during １
８ months follow up after micro-TESE and serum levels of LH at １ to ３ months after micro-TESE

Referenceswere significantly increased from baseline concentrations, but no significant differences were observed in
the levels of LH after ６ months compared to baseline［３８］. Interestingly, FSH and LH concentrations in patients with KS were not significantly changed. The

18

Japanese Journal of Reproductive Endocrinology Vol.14 2009

１．Schlegel （１９９９） PN. Testicular sperm extraction : microdissection improves sperm yield with minimal tissue excision. Hum Reprod １
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Micro-TESE for NOA and hormonal assay

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REVIEW

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Tomomoto ISHIKAWA et al.

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