ORIGINAL PAPER
Nagoya J. Med. Sci. 85. 233–240, 2023
doi:10.18999/nagjms.85.2.233

Infertility treatment for patients having a microdeletionof azoospermic factor (AZF)
Hatsuki Hibi1,2, Miho Sugie1, Megumi Sonohara2,
Noritaka Fukunaga2,3 and Yoshimasa Asada2,3
Department of Urology, Kyoritsu General Hospital, Nagoya, Japan
2
Asada Ladies Clinic, Nagoya, Japan
3
Asada Institute for Reproductive Medicine, Nagoya, Japan

1

ABSTRACTIn genetic causes of male infertility, Y chromosome microdeletions are the second most common after
Klinefelter’s syndrome. Although sperm recovery rate is relatively high for subjects with azoospermic
factor (AZF) c chromosome microdeletion, intracytoplasmic sperm injection (ICSI) results using retrieved
sperm has been reported to be poor. We retrospectively examined the infertility treatment for subjects withAZF microdeletion. From October 2017 to September 2020, chromosomal examination of 67 azoospermic
subjects and 12 cryptozoospermia were performed. Of these, twenty-three subjects (29.1%) had AZF
microdeletion. Twelve subjects with AZFc microdeletion and one subtype with unknown classification(Ym-9; P3 deletion) received sperm retrieval surgery due to azoospermia. Two subjects obtained motile
sperm by microscopic epididymal sperm aspiration (MESA) and four subjects by microscopic testicularsperm extraction (micro-TESE). Pregnancy and healthy delivery were achieved in 6 of 14 subject (42.9%;
including one twin) using ICSI. This was comparable with previous reports. Since there were two casesof obstructive azoospermia, we employed MESA to avoid testicular damage. Following observation of
the testis and epididymis under operative microscope, a decision was made to perform sperm retrieval
surgery to avoid unnecessary testicular damage. Furthermore, since AZFc microdeletion is passed to thenext generation, long term follow-up is necessary.
Keywords: AZF microdeletion, azoospermia, cryptozoospermia, MESA, micro-TESE
Abbreviations:
AZF: azoospermic factor
ICSI: intracytoplasmic sperm injection
MESA: microscopic epididymal sperm aspiration
micro-TESE: microscopic testicular sperm extraction
NOA: non-obstructive azoospermia
OA: obstructive azoospermiaThis is an Open Access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International
License. To view the details of this license, please visit (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Received: February 3, 2022; accepted: May 19, 2022
Corresponding Author: Hatsuki Hibi, MD
Department of Urology, Kyoritsu General Hospital, 4-33 Goban-cho, Atsuta-ku, Nagoya 456-8611, Japan
Tel: +81-52-654-2211, Fax: +81-52-651-7210, E-mail: hibih@quartz.ocn.ne.jp233Hatsuki Hibi et al

INTRODUCTION
Male factor infertility accounts for almost half of the cases in a couple desiring a child.
These male factors problems can be ascribed to infection, immunological factors, anatomicalmalformations, or environmental insult. Besides these factors, genetic abnormalities can also
cause male infertility. In conjunction with the use of intracytoplasmic sperm injection (ICSI) andsperm retrieval technique, patients with chromosomal abnormality are now able to conceive.1,2 In
addition, recent studies have shown that spermatozoa can be retrieved from men with azoospermic
factor (AZF) c microdeletion, thus increasing the chances of conception.3,4
Since patients with AZF microdeletion are generally considered as having non-obstructive
azoospermia (NOA), microscopic testicular sperm extraction (micro-TESE) is employed for sperm
extraction surgery. In the present study, we retrospectively evaluated the clinical characteristics,
sperm retrieval rates, and birth rates for patients with Y chromosome microdeletions in our
institute.

PATIENTS AND METHODS
From October 2017 to September 2020, we performed chromosomal examination for 67
azoospermic subjects and 12 cryptozoospermia (defined as containing less than 1 million sperms
per mL of ejaculate and occasionally zero sperm count) in Asada Ladies Clinic. Patients’ characteristics are shown in Table 1. Physical examination revealed bilateral absent vas deferens in one
subject. Clinically prominent varicocele was not observed. One azoospermic subject had historyof chronic myeloid leukemia (CML) treated with chemotherapy and bone marrow transplantationfrom his sibling at nine-years-old. Sperm retrieval surgery underwent to 13 azoospermic subjects
and one cryptozoospermic subject who could not cryopreserve sperm after repeated ejaculation.
ICSI was attempted by using surgically retrieved or ejaculated, and evaluated the result ofpregnancy and delivery.
Y chromosome microdeletions obtained from peripheral blood lymphocytes were tested ata clinical laboratory (Integrated GENETICS). The analysis system is comprised of the primer
which is specific for 20 kinds of sequence tagged sites (STS). These primers amplify a DNA
Table 1

Patients’ characteristics

n=23
Age (year)

35 (25–54)

Spouse age (year)

32 (25–43)

Testicular volume (right/ left) (mL)

8 (2–20) / 7 (2–18)

LH (mIU/mL)

6.5 (2.3–27.1)

FSH (mIU/mL)

16.0 (3.7–51.7)

Testosterone (ng/mL)

2.80 (1.16–6.70)

Zinc (μg/dL)

84 (62–131)

BMI (Kg/m )23.1 (19.3–27.8)

2Each data was presented as median.
LH: luteinizing hormone
FSH: follicle stimulating hormone
BMI: body mass index
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Treatment for AZF microdeletionfragment by the polymerase chain reaction (PCR) method from a Y chromosome-specific domain.
The presence or absence of each Y specific sequence and the presence of an internal control isdetermined by gel electrophoresis and ethidium bromide staining. This test was developed andits performance characteristics determined by Esoterix Genetic Laboratories, LLC.

RESULTS
Amongst 67 azoospermic and 12 cryptozoospermic subjects, 23 (29.1%) subjects showed AZF
microdeletion. Type of AZF microdeletions were AZFa in 2, AZFb (1), AZFb+c (1), AZFc (18),and unknown classification as AZF Ym-9 (P3 deletion) microdeletion (1), respectively. Correlation
among semen analysis, chromosomal G band, and type of AZF microdeletion are shown in Table
2. Regarding to subtype of AZFc microdeletion, Ym-12 gr/gr microdeletion was most common
in 12 subjects, and Ym-11 b2/b4 microdeletion (1), unknown (3), respectively.
Table 2Semen analysis, chromosomal G band and type of AZF microdeletion

Semen analysis (n)Azoospermia (19)G bandType of AZF microdeletion (n)46XY/46XY inv(9)(p11q13)

AZFa (2)46XY

AZFb (P5/proximal P1) (1)

46,X,der(Y)(Ypter→Yq11.23::Yp11.2→Ypter)

AZFb+c (1)46XY

AZF Ym-9 (P3) (1)

46XY/ 46XY inv(9)(p12:q13)

AZFc unknown subtype (2)46XY

AZFc Ym-12 gr/gr (12)46XY

AZFc Ym-12 gr/gr (2)Cryptozoospermia (4)46XY

AZFc Ym-11 b2/b4 (1)46XY

AZFc unknown subtype (1)AZF: azoospermic factor

Sperm retrieval surgery
A total of 14 subjects, 13 with azoospermia and one cryptozoospermia underwent sperm
retrieval surgery. Type of AZFc microdeletions for azoospermia were Ym 12 gr/gr in ten,
unknown in two, and AZF Ym-9 (P3 deletion) in one. One cryptozoospermic subject showeda Ym 12 gr/gr microdeletion. Of the 13 azoospermic subjects, 11 underwent micro-TESE andmotile sperm were recovered in 4 cases (36.4%) including one with a history of CML in
infancy. Since two azoospermic subjects showed dilated epididymal tubule under an operating
microscope, we employed microscopic epididymal sperm aspiration (MESA), and both cases
recovered motile sperm. Of these, the subject with AZF Ym-9 (P3 deletion) preoperatively wasdiagnosed as having congenital absence of vas deferens by careful palpation, and another had
who showed AZFc Ym-12 gr/gr microdeletion had tentatively diagnosed an epididymal obstruction
because of normal testicular volume and gonadotropins. On the other hand, one cryptozoospermia
who failed cryopreservation of ejaculated sperm after repeated trials received micro-TESE andrecovered motile sperm.
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Hatsuki Hibi et al

ICSI results
One patient with cryptozoospermia of unknown AZFc subtype had a healthy girl by ICSI using
cryopreserved ejaculated sperm. On the other hand, four pregnancies and subsequent deliveries
were obtained by TESE-ICSI. Of these, a cryptozoospermic subject who underwent TESE had
twin healthy girls. Two of the MESA-ICSI subjects had the birth of a healthy boy and girl.
Thus, pregnancy and delivery were achieved in 6 of the 14 subjects (42.9%) who underwent
surgical sperm retrieval. Two boys and five girls (including one twin) were born. Details of AZF
subtypes, sperm retrieval surgery, and ICSI results are shown in Table 3.

Table 3Case-1

Sperm retrieval surgery and result on each caseType of AZF microdeletion

Surgery

Sperm recovery

Pregnancy/delivery

AZF Ym-9 (P3)

MESA

Yes

Yes/healthy girlCase-2

AZFc Ym-12 gr/gr

m-TESENo–

Case-3

AZFc Ym-12 gr/gr

m-TESENo–

Case-4

AZFc unknown subtype

m-TESE

Yes

Yes/healthy boy

Case-5

AZFc Ym-12 gr/gr

m-TESENo–

Case-6

AZFc Ym-12 gr/gr

m-TESENo–

Case-7

AZFc Ym-12 gr/gr

m-TESE

Yes

No

Case-8AZFc Ym-12 gr/gr

m-TESE

Yes

Yes/healthy girlCase-9AZFc Ym-12 gr/gr

MESA

Yes

Yes/healthy boy

Case-10

AZFc unknown subtype

m-TESENo–

Case-11

AZFc Ym-12 gr/gr

m-TESENo–

Case-12

AZFc Ym-12 gr/gr

m-TESENo–

Case-13

AZFc Ym-12 gr/gr

m-TESE

Yes

Yes/healthy girl*Case-14

AZFc Ym-12 gr/gr

m-TESE

Yes

Yes/healthy girl (twin)*Case-14 was cryptozoospermic subject who failed cryopreservation of ejaculated sperm after repeated trials.
MESA: microscopic epididymal sperm aspiration
m-TESE: microscopic testicular sperm extraction

DISCUSSION
Y chromosome microdeletions are the second most common genetic cause of male infertility
after Klinefelter’s syndrome. The locus defined as AZF in Yq11 contains the genes necessary
for normal spermatogenesis, and microdeletions in this locus have been correlated with maleinfertility. The detailed analysis of the Y chromosome in men with azoospermia or cryptozoospermia has resulted in the identification of three regions of the long arm of the human Y
chromosome, named AZFa, AZFb and AZFc, that are currently deleted in men with otherwise
unexplained spermatogenic failure.5 The importance of careful evaluation of AZF microdeletions
in male infertility before assisted reproduction is clear.6 Distinct histopathology phenotypes werecorrelated with the site of the microdeletion, varying from Sertoli cell only (SCO) syndromein patients with AZFa microdeletions, maturation arrest at meiosis (MA) in cases with AZFb
microdeletions, to hypospermatogenesis in patients with AZFc microdeletions.7,8 Thus, only
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Treatment for AZF microdeletion

subjects with AZFc microdeletion a reconsidered as a candidate for surgical sperm retrieval but
this should not be performed for subjects with AZFa, AZFb, and AZFb+c microdeletions. We
agree with this consideration, and in the present study, we examined sperm retrieval surgery
for AZFc microdeletions except one case of unknown classification as AZF Ym-9 (P3 deletion)
microdeletion. AZFc microdeletion is to cause of spermatogenesis disorders due to mainly b2/b4
deletion. On the other hand, partial deletion of AZFc is divided into AZFc gr/gr deletion and
AZFc b2/b3, and subjects with AZFc gr/gr microdeletion in Japan is present in almost 30% of
all men.9 Thus, there are various patterns of partial deletion of AZFc, and the clinical pictureis also different.
According to the practice committee of the American Society of Reproductive Medicine, theprevalence of Y chromosome microdeletion may be as high as 2% in the general population of
unselected men.10 On the other hand, the European academy of andrology defines the prevalenceof AZF microdeletion in unselected men to be far lower, around 1 in 4000 (0.025%).11 A recent
meta-analysis of over 10,000 North American men found that while 5% of cryptozoospermic
patients had an AZF microdeletion, the prevalence of these same deletions was less than 1%
amongst men with normozoospermia.12 A large scale Japanese study screened 1030 infertile
Japanese men for Y chromosome microdeletion, yielding a prevalence of nearly 7% including
all type of AZF microdeletion in the population made up almost exclusively of severely oligozoospermic or azoospermic men. Among the 1030 patients, 4 (5.7%), 4 (5.7%), 10 (14.3%),
and 52 (74.3%) had AZFa, AZFb, AZFb+c, and AZFc microdeletions, respectively.13 The ratioof our subjects with AZF microdeletion was high (23/79=29.1%) when compared with previous
data, however, the ratio of AZFc microdeletion was similar (18/23=78.3%).
Iijima et al reported that the sperm recovery rate (SRR) of micro-TESE in patients with AZFc
deletions was significantly higher than that in those without AZF deletions (60.0% vs 28.7%,
P=0.04). Regarding to subtype of AZFc, in Ym-11 gr/gr deletion, SRR was 18.7%, which was
lower than that in those without gr/gr deletion, but was not statistically significant.13 Tsujimura etal reported that among 60 patients with NOA, the spermatozoa retrieval rate for patients with Y
chromosome microdeletion was similar to that of patients without Y chromosome microdeletion(33.3% vs 37.0%).14 Choi et al also reported that the sperm retrieval rate was similar between
patients with no microdeletion and Y chromosome microdeletion (25.6% vs 26.6%, p=0.298).15 Of
the 13 subjects who underwent sperm retrieval surgery in our study, 6 (46.2%) subjects achieved
motile sperm recovery (MESA 2/2=100%, micro-TESE 4/11=36.4%). Their subtypes were AZFc
Ym-12 gr/gr microdeletion in four, Ym-9 (P3 deletion) in one, and unknown in one. Thus, thecorrelation of the successful motile recovery with the AZFc subtype seems to be unclear.
Yamaguchi et al concluded in a Japanese study analysis that although successful sperm
retrieval was high, ICSI results, especially the fertilization rate was low. When compared withthe control group, the fertilization rate was significantly lower in the testicular group with AZFc
microdeletions (43.7% vs 53.6%, P <0.001).16 On the other hand, spermatozoa retrieved frommen with AZFc deletions when used for ICSI, produce viable embryos and pregnancy at similar
rates as spermatozoa of men without AZFc microdeletions.17 Nickkholgh et al also reported that
AZFc microdeleted spermatogonia behave very similar to normal spermatogonia in vitro and show
equal levels in expression of spermatogonial and differentiation markers as spermatogonia from
non-deleted control men. They concluded that this indicates the treatment of men with AZFc
microdeletions by propagating their spermtogonial stem cell in vitro and autotransplanting themback to the testis is potentially feasible treatment option to restore their fertility.18 In our study,
pregnancy and healthy delivery were achieved in 6 of 14 subject (42.9%; including one twin)using motile sperm obtained by ejaculated, MESA, and micro-TESE. This was comparable withmentioned above previous reports.
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Hatsuki Hibi et al

Although sperm retrieval rate for the subjects with AZFc microdeletion was similar upon
researcher, pregnancy rate was much different.3,4,14-17 Thus, ICSI results for subjects with AZFc
microdeletion are still controversial and accumulation of future cases is necessary.
Azoospermia is classified as either “obstructive azoospermia (OA)” or “NOA,” mainly according to the FSH value, testicular volume, chromosomal evaluation, and past history. Since
subjects with AZFc microdeletion are considered as NOA, micro-TESE has been employed
for sperm retrieval surgery. However, in our case, two subjects who underwent MESA showed
one was epididymal obstruction, and another was absent of vas deferens. Their type of AZF
microdeletion was AZFc Ym-12 gr/gr, and AZF Ym-9 (P3 deletion). Thus, it should be consideredthat azoospermia has a different pathology from AZF microdeletion. Although MESA requires
microsurgical skill, aspirated MESA specimen does not have any special requirements, such as
mincing the tissue. It leads to a reduction in the amount of laboratory work that is needed forcryopreservation. Furthermore, MESA results in better fertilization and pregnancy rates than
TESE.19 van Wely et al also reported that in the first ICSI cycles of couples with obstructive
azoospermia, the use of epididymal spermatozoa resulted in a significantly higher live birth rate
than did the use of testis spermatozoa.20 There is concern about the long-term complications
including of testicular damage by TESE namely testicular atrophy and decreased testosterone.
Testosterone is a lifelong important hormone not only at the time of fertility potential. Since
MESA does not require cutting the testis, it does not cause cellular damage that could leadto a decrease in testosterone. We believe that MESA should be employed for OA to avoid
unnecessary testicular damage.
The AZF test was considered necessary to avoid unnecessary surgery by finding AZF otherthan AZFc, and in the case of AZFc, to know before surgery that AZFc will be transmitted to
the next generation of boys. The possibility of sperm recovery by the subtype of AZFc remained
unclear from this study because the number of cases is small. However, long term follow-up isnecessary including an examination of fertility in the next generation.

CONCLUSIONS
Pregnancy and delivery by ART can be expected if sperm are obtained even in the case of
AZF microdeletions. Subjects with AZFc microdeletion were usually regarded as NOA, but OA
was also apparent in this study. We must be especially careful of the testis and epididymis
under operative microscope and then to decide the appropriate sperm retrieval surgery to avoid
unnecessary testicular damage. Furthermore, since AZFc microdeletion is inherited to the next
generation in males, long term follow-up is necessary.

ACKNOWLEDGEMENT
The authors thank all of the members of the IVF Laboratory team of the Asada Ladies Clinic
and the staff of the Asada Fertility Research Center, Nagoya, Japan.

DISCLOSURE STATEMENT
Human rights and informed consent statements
All procedures completed were done in accordance with the ethical standards of the responsible
committee on human experimentation (institutional and national), and with the Helsinki DeclaraNagoya J. Med. Sci. 85. 233–240, 2023

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Treatment for AZF microdeletion

tion of 1964 and its later amendments. Informed consent was obtained from all patients for the
purpose of inclusion in this study.

STATEMENT OF ETHICS
The protocol for this research project, including its use of human subjects, was approved bya suitably constituted Ethics Committee. (Our approval number: 2020-17, Date of approval by
the Ethical Review Committee: 2020/9/30)

FUNDING SOURCES STATEMENT
Each author has no COI with regard to this manuscript.

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