You are on page 1of 6

Seminars in Pediatric Surgery (2011) 20, 170-175

Embryology of the testicular descent


Henning C. Fiegel, MD, PhD,a Udo Rolle, MD, PhD,a Roman Metzger, MD, PhD,b
Stefan Gfroerer, MD,a Dietrich Kluth, MD, PhDb
From the aDepartment of Pediatric Surgery, Johann Wolfgang Goethe-University, Frankfurt am Main, Germany; and
b
Department of Pediatric Surgery, University of Leipzig, Leipzig, Germany.

KEYWORDS Numerous researchers studied the morphology of the testicular descent, including the possible function of
Fetal genital the gubernaculum. However, a clear illustration of this process is still missing. The aim of this paper was to
development; illustrate the embryology of the testicular descent in the rat by scanning electron microscopy. In a first phase
Gubernaculum testis; of the intra-abdominal testicular descent, the testis moves actively from the lower pole of the kidney towards
Scanning electron the bladder neck. In a second inguinal phase the testis enters groin and moves in the developing processus
microscopy (SEM); vaginalis peritonei caused by the disappearance of the bulb of the gubernaculums testis.
Testicular descent © 2011 Elsevier Inc. All rights reserved.

Since John Hunter in 1762, numerous researchers studied caudo-medial and ventral. In the rat this phase takes place
the morphology of the testicular descent, including the pos- between ED 16 and ED 21. Initially, the position of the
sible function of the gubernaculum. However, a clear illus- testis is located in the region of the lower kidney pole
tration of this process is still missing.1 The aim of this paper (Figure 2A; ED 16). Similarly, the anlage of epididymis
is to document the morphology of testicular descent in the develops from the mesonephric ridge and a gubernaculum
rat using scanning electron microscopy (SEM). presenting with a “corda” and a “conus” or bulb can clearly
be identified in the region of the bladder. The movement of
the testis from the lower kidney pole towards the bladder
Development of the male inner genital neck is the result of true caudal movement (Figure 2B; ED
17). Later on, the testis reaches the bladder neck (Figure 2C;
In the early fetal period, a clear distinction of the sex from ED 18). Subsequently, the testis descents downwards from
morphologic details of the genital anlage is not possible the region of the bladder neck (Figure 2D; ED 19) lateral to
(Figure 1A; embryonic day [ED] 15). The genital anlage is the bladder (Figure 2E; ED 20) until it reaches the region
located medially to the mesonephric ridge. At ED 16, a of the pelvis (Figure 2F; ED 21). In this phase, clear signs
distinct morphology of the male testis develops from a of an active role of the gubernaculum are missing.
shortening and thickening of the genital anlage (Figure 1B).
The gubernaculum is now obvious in male embryos.

Inguinal descent of the testis


Intra-abdominal descent of the testis
In a second phase of descent (inguinal/scrotal descent) the
In a first phase of testicular descent (intra-abdominal de-
formation of the processus vaginalis peritonei takes place
scent) the testis moves from cranio-lateral and dorsal to
while the testis descends into the inguinal/scrotal region.
This takes place between ED 22 and day (D) 2 after birth
Address reprint requests and correspondence: Henning C. Fiegel, MD,
PhD, Department of Pediatric Surgery, Johann Wolfgang Goethe-University in the rat. First the processus vaginalis peritonei (PVP)
of Frankfurt, Theodor-Stern-Kai 7, D-60590 Frankfurt am Main, Germany. develops. At the same time, a thickening of the bulb of
E-mail: henning.fiegel@kgu.de. the gubernaculum is observed (Figure 3A; ED 21.5).

1055-8586/$ -see front matter © 2011 Elsevier Inc. All rights reserved.
doi:10.1053/j.sempedsurg.2011.03.007
Fiegel et al Embryology of the Testicular Descent 171

held responsible for the downward movement of the testis.


Instead, a tension of the gubernaculum would cause a kink-
ing of the anlage of the epididymis, as depicted schemati-
cally in Figure 4B. Thus, a real tension force of the guber-
naculum would be unlikely, causing a downward movement
of the testis during the first phase of intra-abdominal testic-
ular descent. In addition, the epididymis enters the PVP
before the testis. Traction of the gubernaculum to the testis
at this stage would not be possible. Conversely, an increase
of intra-abdominal pressure may cause the movement of the
testis into the PVP.
In the rat, just before the development of the PVP, a
straight gubernaculum is observed (Figure 5A; ED 21.5)
while the testis is still positioned at the bladder region.
When the PVP develops, the testis follows the anlage of
epididymis into the PVP (Figure 5B; ED 22). Of note is that
at this time the corda of gubernaculum shows a curved
shape. In the last phase of the inguinal descent, the testis is
completely embedded in the anlage of the epididymis, when
moving into the PVP (Figure 5C, D 1). Thus, intra-abdom-
inal pressure leading to a coiling of the gubernaculum and
simultaneous regression of the gubernacular bulb is more
likely to cause the inguinal descent of the testis than a
tension of the gubernaculum (Figure 5D). Thus, an active
role of the gubernaculum during the first phase of testicular
descent seems unlikely, while our observations underline
the “transformation theory” of the gubernacular bulb.

Discussion
Figure 1 Anlage of the genital is shown at ED 15 (A) and ED
Our documentation showed that in the first phase (transab-
16 (B) in the rat (ventral view via SEM). At ED 15 (A) the sex
determination of the genital anlage is still morphologically indis- dominal phase) the testis moved from the region of the
tinguishable. At ED 16 (B) the testis can clearly be identified. G, lower kidney pole downward and reached finally the ingui-
gonadal anlage; T, testis, MR, mesonephric ridge. nal region. In anatomic studies in human and mouse fetuses
a movement of the testis towards the inguinal region was
doubted, because it may be effected by an ascent of the
Subsequently, the anlage of epididymis moves from the kidney.2,3 In our serial investigations, we document an ac-
abdominal cavity into the PVP (Figure 3B; ED 22). At this tive movement of the testis downward to the bladder neck.
time, a regression of the bulb of the gubernaculum can be In this phase, signs of traction of the corda of the guber-
observed, which causes a further downward movement of naculum on the testis were missing. This finding is contrary
the anlage of epididymis (Figure 3C; D1) and is followed by to anatomical studies of human fetuses in which the authors
the entrance of the testis in the PVP (Figure 3D, D 1.5). For proposed an important role of the attachment of the guber-
the inguinal testicular descent the regression of the guber- naculum and the increasing size of the gubernaculum in the
nacular bulb plays a crucial role for the downward move- abdominal phase of the testicular descent to direct the testis
ment of the testis, as depicted schematically in Figure 3E. towards the inguinal region.4
In the second phase (inguinal phase), it was observed that
the regression of the bulb of gubernaculum lead to the
formation of the PVP. In a study in fetal calfs also a
The role of the gubernaculum testis for the swelling of the bulb of gubernaculum could be shown,
testicular descent which lead to a dilatation of the inguinal ring before the
inguinoscrotal descent of the testis.5 Three main aspects
In the beginning of the intra-abdominal phase, the corda of were important for leading the testis towards the inguinos-
the gubernaculum is rather attached to the anlage of the crotal region at the end of the intra-abdominal phase: (1) the
epididymis than to the lower pole of the testis (Figure 4). growth of the bulb of gubernaculum, (2) the central regres-
Thus, traction of the gubernaculum cannot sufficiently be sion of the gubernaculum, and (3) the intra-abdominal pres-
172 Seminars in Pediatric Surgery, Vol 20, No 3, August 2011

Figure 2 Testis and gubernaculum between ED 16 and ED 22 are shown in a male rat (ventral view via SEM). The testis lies in the region
of the lower kidney pole at ED 16 (A). Half a day later, the testis starts to move ventrally and downwards (B, ED 17; 2 C, ED 18), reaching
the region of the bladder neck (D, ED 19). Finally, the testis is moving from the bladder neck downwards (E, ED 20) towards the inguinal
region (2 F, ED 21). K, kidney; T, testis; AE, anlage of epididymis; GB, bulb of gubernaculum; BL, bladder.
Fiegel et al Embryology of the Testicular Descent 173

Figure 3 At ED 22, the development of the PVP begins in rats (A). At this time, the bulb of the gubernaculum is still thickening. Half
a day later, the anlage of epididymis enters the PVP first followed by a passive movement of the testis (B; D 0.5). At this time, the regression
of the gubernacular bulb begins. The testis follows the anlage of epididymis entering into the PVP (C; D 1). Finally, the gubernacular bulb
is fully regressed and the anlage of epididymis and the testis lie within the PVP (D; D 1-5). The movement of the testis into the PVP is
strongly associated with the regression of the bulb of gubernaculum as depicted in the scheme (E). T, testis; AE, anlage of epididymis; GB,
bulb of gubernaculum.
174 Seminars in Pediatric Surgery, Vol 20, No 3, August 2011

Figure 4 In the beginning of the intra-abdominal phase the


corda of the gubernaculum is attached rather to the AE than to the
lower pole of the testis (A). Thus, a tracing force of the gubernac-
ulum would not sufficiently cause the testis to move downward.
Instead, a tension of the gubernaculum would cause a kinking of
the anlage of the epididymis, as depicted schematically in panel B.
T, testis; AE, anlage of epididymis; GB, bulb of gubernaculum;
BL, bladder.

sure.6 In rat fetuses the gubernacular attachment of the testis


and the intra-abdominal pressure were demonstrated to have
synergistic effects on the testicular descent.7 The PVP was
first entered by the epididymis, followed by the testis. In
addition, the testis reached the scrotum passively in this

Figure 5 In the rat just before the development of the PVP, a


straight gubernaculum can be observed (A; ED 21.5) while the
testis still is positioned in the bladder region. When the PVP
develops the testis follows the anlage of epididymis passively into
the PVP (B; ED 22). Of note is that at this time the corda of
gubernaculum shows a curved shape. In the last phase of the
inguinal descent the testis is completely embedded in the anlage of
the epididymis when moving into the PVP (C; D 1). Thus, intra-
abdominal pressure leading to a coiling of the gubernaculum and
simultaneous regression of the gubernacular bulb is here likely to
initiate the inguinal descent of the testis than a tension of the
gubernaculum, as depicted in the scheme in panel D. T, testis; AE,
anlage of epididymis; GB, bulb of gubernaculum; BL, bladder.
Fiegel et al Embryology of the Testicular Descent 175

phase. The mechanisms of the descensus testis are multi- 2. Van der Schoot P. Doubts about the first phase of testis descent in the
factorial. It is known that the first transabdominal descent is rat as a valid concept. Anat Embryol 1993;187:203-8.
3. Shono T, Ramm-Anderson S, Hutson JM. Transabdominal testicular
independent of androgens.8 However, it has been proposed
descent is really ovarian ascent. J Urol 1994;152:781-4.
that HOXA-10 and insulin-like factor 3 are possible regu- 4. Heyns CF. The gubernaculum during testicular descent in the human
lators of the abdominal testicular descent.9-11 In the ingui- fetus. J Anat 1987;153:93-112.
noscrotal phase, the swelling of the bulb and shortening of 5. Hullinger RL, Wensing CJ. Descent of the testis in the fetal calf. A
the corda of gubernaculum may result in the scrotal descent summary of anatomy and process. Acta Anat (Basel) 1985;121:
of the testis. In this phase androgens, the calcitonin gene- 63-8.
6. Wensing CJ. The embryology of testicular descent. Horm Res 1988;
related peptide released from the genitofemoral nerve and
30:144-52.
the epidermal growth factor were found to be regulators of 7. Attah AA, Hutson JM. The role of intra-abdominal pressure in cryp-
the testicular descent.12,13 torchidism. J Urol 1993;150:994-6.
8. Shono T, Ramm-Anderson S, Goh DW, et al. The effect of flutamide
on the testicular descent in rats examined by scanning electron mi-
Conclusions croscopy. J Pediatr Surg 1994;29:839-44.
9. Zimmermann S, Steding G, Emmen JM, et al. Targeted disruption of
In conclusion in the first phase of the intra-abdominal tes- the Insl3 gene causes bilateral cryptorchidism. Mol Endocrinol 1999;
13:681-91.
ticular descent, the testis moves actively from the lower pole
10. Kubota Y, Nef S, Farmer PJ, et al. Leydig insulin-like hormone,
of the kidney towards the bladder neck. Then, in the second gubernacular development and testicular descent. J Urol 2001;165:
phase the testis moves into the developing processus vagi- 1673-5.
nalis peritonei caused by the disappearance of the bulb of 11. Feng S, Bogatcheva NV, Truong A, et al. Over expression of insulin-
the gubernaculums testis. like 3 does not prevent cryptorchidism in GNRHR or HOXA10 defi-
cient mice. J Urol 2006;176:399-404.
12. Shono T, Suita S, Kai H, et al. The effect of a prenatal androgen
disruptor, vinclozolin, on gubernacular migration and testicular de-
References scent in rats. J Pediatr Surg 2004;39:213-6.
13. Clarnette TD, Hutson JM. The genitofemoral nerve may link testicular
1. Heyns CF, Hutson JM. Historical review of theories on testicular inguinoscrotal descent with congenital inguinal hernia. Aust N Z
descent. J Urol 1995;153:754-67. J Surg 1996;66:612-7.

You might also like