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Journal of Indian Association of Pediatric Surgeons
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Year : 2023  |  Volume : 28  |  Issue : 6  |  Page : 465-471

Comparison of high spermatic vessel ligation and low spermatic vessel ligation in an undescended model of rat testis

1 Department of Pediatric Surgery, AIIMS, New Delhi, India
2 Department of Pathology, AIIMS, New Delhi, India
3 Department of Reproductive Biology, AIIMS, New Delhi, India

Date of Submission19-Jan-2023
Date of Decision28-Jun-2023
Date of Acceptance23-Jul-2023
Date of Web Publication02-Nov-2023

Correspondence Address:
Murali Krishna Nagendla
Sravani Multispeciality Hospital, Cyber Hills, Hyderabad - 500 034, Telangana
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jiaps.jiaps_14_23

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Aims: The aim of this study was to compare the immediate and long-term outcomes after high spermatic vessel ligation (HSVL) and low spermatic vessel ligation (LSVL) in a high undescended testis (UDT) model in rats.
Materials and Methods: A prospective randomized controlled study was conducted on 24 male Wistar rats. The rats were randomly divided into three groups. Group A underwent a sham laparotomy and acted as the control. Group B underwent HSVL of both testicular vessels. Group C underwent LSVL of both testicular vessels. Each group was again subdivided into two subgroups. One sub-group underwent blood collection and testicular biopsy of both testes 24 h after the procedure to demonstrate immediate changes. Other subgroups underwent blood sample collection and testicular biopsy of both testes on day 50 following the procedure for hormonal changes and long-term changes.
Results: All the testes in HSVL showed atrophy (100%) in the long term, whereas LSVL showed atrophy in 12.5% of testes, even though both groups showed adequate neovascularization. Testes in HSVL showed poor bleeding on incision at both 24 h and day 50. On histology, 75% of testes in HSVL showed complete necrosis, and 50% in LSVL showed partial necrosis at 24 h. On day 50, all the testes in HSVL (100%) showed complete necrosis with dystrophic calcification, whereas all the testes in LSVL showed normal histology with good maturation of seminiferous tubules. There was no significant difference in testosterone levels between both groups.
Conclusions: Both immediate and long-term changes following LSVL showed an increase in blood flow to the testis after ligation through collaterals and reverses early ischemic changes to the testis. Given the higher testicular atrophic rate after HSVL, LSVL or at least low ligation can be preferred for the management of high intra-abdominal UDT.

Keywords: High spermatic vessel ligation, Johnsen's score, low spermatic vessel ligation, testis morphology, testosterone assay, undescended testis

How to cite this article:
Nagendla MK, Jain V, Agarwala S, Srinivas M, Sharma M C, Gupta S. Comparison of high spermatic vessel ligation and low spermatic vessel ligation in an undescended model of rat testis. J Indian Assoc Pediatr Surg 2023;28:465-71

How to cite this URL:
Nagendla MK, Jain V, Agarwala S, Srinivas M, Sharma M C, Gupta S. Comparison of high spermatic vessel ligation and low spermatic vessel ligation in an undescended model of rat testis. J Indian Assoc Pediatr Surg [serial online] 2023 [cited 2023 Nov 29];28:465-71. Available from: https://www.jiaps.com/text.asp?2023/28/6/465/389317

   Introduction Top

Undescended testis (UDT) is one of the most common congenital urogenital anomalies in children. It occurs in approximately 3% of the newborn at term and 33%–45% of preterm babies. Impalpable UDT accounts for 5%–28% of UDT. Among the impalpable testis, 50%–60% are intra-abdominal or canalicular, 30% are atrophic or rudimentary, and the rest 20% are absent. Management of these intra-abdominal testes is most challenging due to the main constraint factor of short testicular vessel length for a single-stage orchidopexy.

Most performed surgical procedures to bring high UDT to the scrotal sac involve the division of spermatic vessels. The various types of spermatic ligation are high spermatic vessel ligation (HSVL)[1] and low spermatic vessel ligation (LSVL).[2] Both procedures are based on the division of testicular vessels, followed by the development of collaterals and neovascularization to the testis. HSVL is the most performed procedure for the management of high UDT.

Results with the Fowler Stephen procedure were variable. Many studies on long-term effects after the Fowler–Stephen procedure showed a lower success rate (76%)[3] and higher testicular atrophy (17%).[4] Koff and Sethi[2] showed a lower success rate with the Fowler Stephen procedure and proposed a new technique of LSVL and showed a success rate of 97% at 1 month and 93% at the end of 1-year postprocedure.

Similarly, Docimo[3] showed a failure (atrophy and retraction) rate of 31.5% after the staged Fowler–Stephen procedure. Further studies by Stec et al.[5] also demonstrated a failure rate (atrophy) of 37% and 32% following single-stage or two-stage Fowler Stephen orchidopexy. Various studies by Hvistendahl and Poulsen[6] and Baker et al.,[7] also reported atrophy rates of 14% (65 testes) and 10% (58 testes) respectively. There is no single evidence or study to compare the efficacy of one procedure over the other (HSVL vs. LSVL) in humans.

The present study was conducted in a rat model because it resembles human reproductive anatomy, physiology, and ease in the procedure, and both procedures were compared in a UDT model. A shorter interval to puberty in rats had the advantage to observe the testicular changes at puberty, which cannot be studied in humans. Many comparative studies were published in rat models between single and two stages of HSVL, but not of HSVL with LSVL till now.

   Materials and Methods Top

This prospective randomized controlled study was conducted on 24 male Wistar rats aged 20–25 days (prepubertal) with a weight of 80–90 g each. Prepubertal rats will have testis inside the abdomen and the testis descends before puberty. Puberty attains in rats along with spermatogenesis at 42–45 days of life and attains optimum production by day 70–75 of life. The rats were randomly divided into three groups of eight each and each group was again divided into two subgroups of 4 rats. The rats in Group A underwent sham laparotomy and acted as a control group. Whereas Group B underwent high spermatic vessel ligation of both testicular vessels and Group C underwent low spermatic vessel ligation of both testicular vessels in prepubertal-age (20-25 days) rats ( [Figure 1]. Schematic diagram of study). Laparotomy with testicular biopsy and blood sampling was taken from half of the rats (A1, B1, C1) in each group at 24 h and the other half (A2, B2, C2) on day 50 (corresponding to day 70–75 of life) following ligation or sham laparotomy.
Figure 1: Schematic diagram of the study

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In Group A rats, testes were brought outside and repositioned intraperitoneally [Figure 2]. In Group B rats, bilateral testicular vessels were traced up to the renal pedicle and ligated just below the renal pedicle with a 5–0 Silk suture [Figure 2]. In Group C rats, bilateral testicular vessels were ligated just above the testes [Figure 2].
Figure 2: Procedure on rats: Upper-sham laparotomy, Middle-high spermatic vessel ligation, Lower-low spermatic vessel ligation

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Procedure at 24 h (Group A1, Group B1, Group C1) and procedure at day 50 (Group A2, Group B2, Group C2)

External morphological features of testes like the size, and color of testes post 24 h after ligation, and the neovascularization pattern at day 50, were observed. The Sham laparotomy group (Group A) acted as the control. Testes were incised, and bleeding from the testes was observed. In all rats, both the testes were excised and sent for biopsy, and rats were reared separately for life (No rats were sacrificed during or after the procedure). Findings of apoptosis, necrosis, and dystrophic calcification were noted on the histological examination of slides. The structure of seminiferous tubules was noted. All the slides were observed for maturation of the testis, particularly in day 50 rats. Different stages of differentiation of spermatogonia, spermatocyte, and spermatids were observed.[8],[9] Maturation of the testis was measured by Johnsen testicular biopsy score[10] (TBS). Blood was collected from each rat and a serum testosterone assay was done with ELISA kits. All the groups' serum testosterone results were compared with normal values from the literature (Serum testosterone value at 21-35 days is 0.05- 0.50 ng/ml, and at day 70 is 3-6 ng/ml).[11]

   Results Top


At 24 h: Normal-looking testis were present in Group A. Whereas, in Group B and Group C, both testes were congested and edematous [Figure 3].
Figure 3: Morphology of testis: Upper: 24 h after the procedure, normal testis in sham group versus congested and edematous testis in low spermatic vessel ligation (LSVL) group. Lower: day 50 of the procedure. The sham group testis looks normal, the LSVL test is smaller than the sham group, high spermatic vessel ligation group test is small and atrophic

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On day 50: Bilateral testes were normal in size and shape in the Sham laparotomy group. Whereas all the testes in Group B were smaller in size and atrophic (100%) except one rat (B2.3), which had an atrophic testis on the right and nubbin tissue (without any testicular morphology) on the left side. Group C rats showed near-normal-sized testes except for one, which is smaller in size (12.5%). All the tests in both groups (B and C) showed good neovascularization [Figure 3].

Bleeding from testes

Bleeding from the testis is a subjective observation, considering the sham group as a standard. Compared to the sham group, any bleeding similar is considered good, and anything less as poor bleeding.

At 24 h: All the testes in Group A showed good bleeding on the cut surface. In Group B, 4 out of 8 (50%) testes showed poor bleeding; the rest showed good bleeding on cutting, whereas, in Group C, all the testes except one (12.5%) showed a good bleeding surface.

On day 50: All the testes in Group A showed good bleeding on the cut surface similar to 24 h sub-group. In Group B, 7 out of 7 (one nubbin) (100%) testes showed poor bleeding, and all the testes (100%) showed a good bleeding surface in Group C.

Testosterone values (prepubertal vs. postpubertal)

Mean serum testosterone levels in prepubertal rats (day 20–25 of life) in the sham group, HSVL, and LSVL groups were 0.172 ng/mL (±0.19 ng/mL), 0.052 ng/mL (±0.009 ng/mL) and 0.082 ng/mL (±0.079 ng/mL) respectively. Postpubertal (day 70–75 of life) testosterone values in the sham group, HSVL, and LSVL groups were 5.377 ng/mL (±8.62 ng/mL), 1.09 ng/mL (±0.69 ng/mL), and 2.745 ng/mL (±4.24 ng/mL). In postpubertal rats, there was an increase in testosterone levels compared to prepubertal rats. Serum testosterone levels of both Group B and C had lower values compared to Group A (Group B levels are even lower than Group C). The results analyzed by Student's t-test comparing mean testosterone levels showed no statistical significance (P = 0.20) between both groups (Group A with Group B). Even though there is a quantitative difference in testosterone levels between groups but statistical analysis showed no significant difference between Group A with Group C (P = 0.32) and Group B with Group C (P = 0.24) (significance considered at P < 0.05) [Table 1].
Table 1: Serum testosterone levels pre- and postpubertal rats

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At 24 h: In Group A, testes showed normal tubular architecture of seminiferous tubules [Figure 4], and immature tubules (only spermatocytes were seen) were seen in all specimens. In Group B, three rats showed complete necrotic changes of seminiferous tubules, and the stroma was necrotic with disarray and loss of structure [Figure 4]. One rat in group B (B1.4) showed preserved seminiferous tubule structure and stroma without necrosis. In Group C, two rats showed normal histology (tubular structure and stroma) without necrosis, and the testes from C1.2 and C1.4 rats showed partial necrotic changes, with loss of tubular structure in necrotic areas and normal tubular structure in normal areas [Figure 4]. Mean Johnsen's score in sham, HSVL, and LSVL were 5, 2, and 4 respectively and the low score in HSVL compared to LSVL is explained by postligation reduction of blood supply is paramount in HSVL [Table 2].
Table 2: Histopathological findings of testes at 24 h and on day 50

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Figure 4: Light microscopy of the testis, right upper: Sham group at 24 h showing normal seminiferous tubules, upper-middle: high spermatic vessel ligation (HSVL) group at 24 h showing necrosis, Left upper: LSVL group at 24 h showing mild necrosis of seminiferous tubules, Right lower: Sham group at day 50 showing normal seminiferous tubules and maturation, Lower middle: HSVL group at day 50 showing loss of structure and dystrophic calcification, Left lower: LSVL group at day 50 showing normal seminiferous tubules with maturation

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On day 50: In Group A, the testes had the normal tubular architecture of the seminiferous tubules [Figure 4], and maturation of tubules were seen in all testes. In Group B, all the rats showed complete necrosis with loss of structure of seminiferous tubules, and dystrophic calcification was seen in all [Figure 4]. Whereas in Group C, all the testes except one had minimal tubular necrosis but preserved tubular structure and maturation were seen [Figure 4]. In Group C, one rat (C2.3) testis showed fungal granulomas. Mean Johnsen's score in sham, HSVL, and LSVL were 8.25, 1, and 7, respectively [Table 2].

   Discussion Top

During mobilization of the testis during orchidopexy (impalpable UDT), occasional inadvertent damage may happen to testicular vessels resulting in atrophy of the testis in the long term. In 1959 Fowler and Stephens[1] described the procedure of high ligation of testicular vessels (at the level of the lower pole of the kidney) and observed sustenance of the testis by the development of neovascularization by the collaterals from the artery to Vas and cremasteric vessels. Though HSVL was adopted and initially performed as a single-stage procedure for high intra-abdominal UDT, with poorer long-term results, a staged approach was proposed. A subtle change in the procedure was proposed by Koff and Sethi[2] by low ligation of vessels near the testis. Though both procedures were popular, staged HSVL is the most performed procedure compared to LSVL. But long-term results regarding anatomical changes and functionality of the testis following HSVL are difficult to analyze in humans due to ethical concerns regarding acceptance for testicular biopsy and long follow-up for postpubertal changes.

Hence, a compared study in a similar physiological model was conducted in rats which has a shorter timeline for puberty and so ease for assessment of anatomical changes and pubertal changes. When ischemic changes in the testis were observed, there is a vascular insult postvessel ligation which is both reversible and irreversible. The reversibility of ischemic changes depends on the development of collateral circulation to testis from nearby vessels. At 24 h, immediate changes in the testis reflected the state of balance between ischemia and recovery (following improvement of blood flow from collaterals). Whereas delayed changes (day 50) showed the adequacy of neovascularization between the testis and vessels from Vas and cremasteric vessels. Following the HSVL, irreversible damage to the testis was noted (atrophic changes) inferring ineffective collaterals or poor neovascularization. On the contrary, initial ischemic changes with delayed recovery of testis following LSVL shows effective collateral circulation and neovascularization overcoming the decreased blood flow postligation, as hypothesized by Koff and Sethi.[2] Vessel ligation always compromises blood supply as depicted in both groups as severe congestion and edema initially, but HSVL had higher atrophic rates compared to LSVL where normal morphology of the testis was restored following a brief insult, once again confirming a better blood supply from collaterals, earlier neovascularization, and earlier reversal of the ischemic process. In a similar study, Erçöçen et al.[12] demonstrated severe testicular atrophy following the Fowler Stephen procedure, and the same was affirmed by Sperling et al.,[13] showing 70% of testis were atrophied following the HSVL. Another indirect anatomical parameter to study early and late changes regarding good vascularity is bleeding from the testes. After the Fowler–Stephen procedure, Salman and Fonkalsrud[14] also noticed poor bleeding from the testis and demonstrated bleeding from the testis was less than one-fifth when compared to the controls. We also found a similar poor bleeding pattern following HSVL again asserting that poor neovascularization is not enough to sustain the viability of the testis, while on the contrary LSVL testis showed good bleeding.

Testis will contain both seminiferous tubules for sperm production and Leydig cells for testosterone production. Following the vessel ligation, both cells may respond differently depending on the resistance to ischemia-recovery time. A comparative study of serum testosterone gives both the inference of resistance to vascular insult and better of both procedures. In this study, postpubertal rats in all three groups showed a rise in serum testosterone levels compared to prepubertal controls. Although the postpubertal sham group had a physiological rise, both postpubertal HSVL and LSVL groups had lower levels of serum testosterone compared to the sham group. The lower testosterone values even after the pubertal rise but not attaining the levels of control in both groups are explained by the partial Leydig cell damage due to the ischemic insult. Even though there is a rise in testosterone levels postpuberty, both procedures involve a certain level of damage to Leydig cells at the same time it also proves Leydig cells are more resistant than seminiferous tubules to the ischemia. In an isolated comparative study Pascual et al.,[15] proposed the Leydig cells were more resistant to ischemia than the seminiferous tubules after spermatic vessel ligation. However, Salman and Fonkalsrud[14],[16] noticed no major difference in serum testosterone levels between the Fowler Stephen procedure (0.19 ± 0.31 ng/mL) and the sham group (1.43 ± 0.75 ng/mL). Microscopic studies of the testis following the ligation show the exact architecture, histology, and the extent of damage caused immediately after ligation or in long term for chronic changes. On microscopy, HSVL testes showed large extent necrosis and partial necrosis in the LSVL group immediately. This large extent of necrosis in the HSVL group compared to partial necrosis in the LSVL group is due to the same above-explained vascular phenomenon. As a consequence of the necrosis there will be a distortion of tubular architecture in the testes and the same was endorsed by Huang et al.[16] showing marked distortion of tubular morphology within 2 weeks postprocedure and interstitial fibrosis at 4 weeks. Pascual et al.,[17] noticed focal necrosis of seminiferous tubules in 83% of testes following HSVL after 30 days and elucidated the same inefficient vascularity. Whereas microscopy of postpubertal testes (long-term) showed complete atrophy of testes with dystrophic calcification in the HSVL group proving poor neovascularization not enough for long-term sustenance. Barring from ischemia LSVL testes developed good vascularity and showed normal architecture and maturation. In analogous studies by Kamisawa et al.,[18] severe necrosis of seminiferous tubules and impaired spermatogenesis was noticed following the Fowler-Stephen procedure. Vindicative evidence of damage following the Fowler Stephen procedure was demonstrated by Rosito et al.[19] in terms of reduction in the number of seminiferous tubules, the number of tubules with spermatogonia, the total number of spermatogonia, and the number of spermatogonia per tubular cross-section on histology. Further comprehensive study regarding the haploid cell population in the seminiferous tubules by Srinivas et al.[20] showed a decrease in a haploid cell population with low maturation in both HSVL and LSVL groups. A constant curtailing blood supply to the testis following HSVL may lead to atrophy in the long term as noticed in this study and such changes are substantiated by the study of Gougoudi et al.,[21] who showed testicular atrophy rates of 68% of the testis with severe necrosis of seminiferous tubules. Furthermore, Salman and Fonkalsrud[14] observed varied changes ranging from focal infarcted areas to complete infarct with tubular damage along with a low Johnsen TBS post-Fowler–Stephen procedure compared to the controls in postpubertal rats.

When adoption of similar vessel ligation methods for the management of high UDT in humans may have similar long-term results. As a most commonly performed procedure in humans, HSVL underwent various modifications over time, and instead of vessel ligation at the level of the renal pedicle, most of the vessels were ligated near the testis or a few centimeters away from the testis. Even though such ligation does not label as LSVL, vessels are ligated as low and hence the achieved results in humans are similar to the LSVL group in this study.

   Conclusions Top

Management of high UDT may require the division of spermatic vessels, which can lead to ischemic changes in the testis that may be reversible or irreversible. When comparing both procedures, immediate and long-term changes in the testis after LSVL showed an increase in blood flow to the testis after ligation through collaterals and reverses early ischemic changes to the testis. Given the higher testicular atrophic rate after HSVL, LSVL or at least vessel ligation near the testis can be preferred for the management of high intra-abdominal UDT.

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Conflicts of interest

There are no conflicts of interest.

   References Top

Fowler R, Stephens FD. The role of testicular vascular anatomy in the salvage of high undescended testes. Aust N Z J Surg 1959;29:92-106.  Back to cited text no. 1
Koff SA, Sethi PS. Treatment of high undescended testes by low spermatic vessel ligation: An alternative to the Fowler-Stephens technique. J Urol 1996;156:799-803.  Back to cited text no. 2
Docimo SG. The results of surgical therapy for cryptorchidism: A literature review and analysis. J Urol 1995;154:1148-52.  Back to cited text no. 3
Esposito C, Vallone G, Savanelli A, Settimi A. Long-term outcome of laparoscopic Fowler-Stephens orchiopexy in boys with intra-abdominal testis. J Urol 2009;181:1851-6.  Back to cited text no. 4
Stec AA, Tanaka ST, Adams MC, Pope JC 4th, Thomas JC, Brock JW 3rd. Orchiopexy for intra-abdominal testes: Factors predicting success. J Urol 2009;182:1917-20.  Back to cited text no. 5
Hvistendahl GM, Poulsen EU. Laparoscopy for the impalpable testes: Experience with 80 intra-abdominal testes. J Pediatr Urol 2009;5:389-92.  Back to cited text no. 6
Baker LA, Docimo SG, Surer I, Peters C, Cisek L, Diamond DA, et al. A multi-institutional analysis of laparoscopic orchidopexy. BJU Int 2001;87:484-9.  Back to cited text no. 7
Caneguim BH, Cerri PS, Spolidório LC, et al. Structural alterations in the seminiferous tubules of rats treated with immunosuppressor tacrolimus. Reproductive Biology and Endocrinology 2009;7:19.  Back to cited text no. 8
Huckins C. The spermatogonial stem cell population in adult rats. I. Their morphology, proliferation, and maturation. The Anatomical Record 1971;169:533-57.  Back to cited text no. 9
Johnsen SG. Testicular Biopsy Score Count – A Method for Registration of Spermatogenesis in Human Testes: Normal Values and Results in 335 Hypogonadal Males. Hormone Research in Paediatrics 1970;1:2-25.  Back to cited text no. 10
Noguchi J, Yoshida M, Ikadai H, Imamichi T, Watanabe G, Taya K. Age-related changes in blood concentrations of FSH, LH and testosterone and testicular morphology in a new rat sterile mutant with hereditary aspermia. J Reprod Fertil 1993;97:433-9.  Back to cited text no. 11
Erçöçen AR, Soejima K, Sakurai H, Yenidünya S, Kikuchi Y, Nozaki M. Revascularization of the testis using a vascular induction technique: A potential approach for staged orchiopexy in high-undescended testis. Urol Res 2004;32:1-8.  Back to cited text no. 12
Sperling H, Lümmen G, Schmidt C, Rübben H. Cryptorchidism: Fowler-Stephens procedure or autotransplantation-a new experimental model. Urology 2000;56:886-90.  Back to cited text no. 13
Salman FT, Fonkalsrud EW. Effects of spermatic vascular division for correction of the high undescended testis on testicular function. Am J Surg 1990;160:506-10.  Back to cited text no. 14
Pascual JA, Villanueva-Meyer J, Salido E, Ehrlich RM, Mena I, Rajfer J. Recovery of testicular blood flow following ligation of testicular vessels. J Urol 1989;142:549-52.  Back to cited text no. 15
Huang EJ, Kelly RE Jr., Fonkalsrud EW, Liu HW, Masuda H, Salman FT. Effects of simulated Fowler-Stephens orchiopexy on testicular structure and function in rats. Am Surg 1992;58:153-7.  Back to cited text no. 16
Pascual JA, Villanueva-Meyer J, Rutgers JL, Lemmi CA, Sikka SC, Ehrlich RM, et al. Long-term effects of prepubertal testicular vessel ligation on testicular function in the rat. J Urol 1990;144:466-8.  Back to cited text no. 17
Kamisawa H, Kojima Y, Mizuno K, Imura M, Kohri K, Hayashi Y. Spermatogenesis after 1-stage Fowler-Stephens orchiopexy in experimental cryptorchid rat model. J Urol 2010;183:2380-4.  Back to cited text no. 18
Rosito NC, Koff WJ, da Silva Oliveira TL, Cerski CT, Salle JL. Volumetric and histological findings in intra-abdominal testes before and after division of spermatic vessels. J Urol 2004;171:2430-3.  Back to cited text no. 19
Srinivas M, Kilmartin B, Das SN, Puri P. Prepubertal unilateral spermatic vessel ligation decreases haploid cell population of ipsilateral testis postpubertally in rats. Pediatr Surg Int 2005;21:360-3.  Back to cited text no. 20
Gougoudi E, Pikoulis E, Karavokyros I, Gorgas K, Felekouras E, Georgopoulos S, et al. Outcome of Fowler-Stephens operation for undescended testes: An experimental study. J Androl 2007;28:813-20.  Back to cited text no. 21


  [Figure 1], [Figure 2], [Figure 3], [Figure 4]

  [Table 1], [Table 2]


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