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The effect of detorsion versus orchiectomy following experimental unilateral testicular torsion on the contralateral testis and epididymis: a light and transmission electron microscopic study

Hafez, Manal Shaaban; Makhlouf, Noha A.; Saleh, Hanan A.

The Egyptian Journal of Histology: September 2012 - Volume 35 - Issue 3 - p 620–632
doi: 10.1097/01.EHX.0000418133.61834.50
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Introduction Testicular torsion is a true surgical emergency that results from rotation of the testis around the axis of the spermatic cord.

Aim of the study To determine the microscopic changes in the contralateral testis and epididymis following corrective detorsion or orchiectomy. It was also aimed to determine which of the two procedures better preserves the testicular structure.

Materials and methods Young adult rats (2–3 months old) were divided into three groups. Group I included sham-operated animals. group II included animals that were subjected to left testicular torsion for 2 h. Then, they were subjected to ipsilateral detorsion, followed by a 1-week recovery period. group III included animals that were subjected to left testicular torsion for 2 h as in group II. Then, the animals were subjected to left testicular orchiectomy, followed by a 1-week recovery period. At the end of the experiment, specimens from the right testes and epididymi were taken and prepared for light and transmission electron microscopic study.

Results Group II showed distortion of the seminiferous tubules with loss of the normal architecture. The spermatogenic cells were disorganized, degenerated, and separated from the underlying basement membranes. Many multinucleated giant cells were observed in some seminiferous tubules. The lumena of some tubules contained acidophilic necrotic material and sloughed germ cells, with the absence of sperm in most of them. The interstitial spaces were wide and hypercellular. The tubules of the epididymis were filled with necrotic remnants. By electron microscopy, the spermatogenic cells appeared irregular, distorted, and their cytoplasm contained many vacuoles. Group III showed a better tubular architecture in relation to group II.

Conclusion It was concluded that orchiectomy following testicular torsion better preserved the structure of the contralateral testis and epididymis as compared with detorsion.

Department of Histology, Faculty of Medicine, Ain Shams University, Cairo, Egypt

Correspondence to Noha A. Makhlouf, Assistant Prof of Histology, Faculty of Medicine, Ain Shams University, Cairo, Egypt Tel: 29298406; 01001130563; e-mail: nohamakhlouf@yahoo.com

Received February 16, 2012

Accepted April 18, 2012

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Introduction

Testicular torsion is a true surgical emergency that results from rotation of the testis around the axis of the spermatic cord [1]. This results in ischemia of the testis because of occlusion of the blood vessels. Rapid diagnosis and immediate surgical treatment are essential to avoid permanent testicular damage and infertility [2].

The incidence of testicular torsion is the highest in males younger than 25 years of age. All prepubertal and young adult males with acute scrotal pain should be considered to have testicular torsion until proven otherwise [3].

Torsion usually occurs in the absence of any precipitating event and only 4–8% of cases result after trauma. Other predisposing factors to testicular torsion include an increase in testicular volume, which occurs with puberty, testicular tumors, testicles with horizontal lie, and a spermatic cord with a long intrascrotal portion [4].

According to Kar et al., unilateral testicular torsion (UTT) is followed by reduced blood flow not only in the ipsilateral testis but also in the contralateral testis. This is associated with overproduction of reactive oxygen species (ROS) and tissue damage [5].

There have been many clinical [6,7] and experimental studies [5,8,9] on contralateral testicular injury following UTT. There is a controversy regarding the effects of ischemia–reperfusion (I/R) on the ipsilateral and the contralateral testes after unilateral torsion and detorsion of the spermatic cord [5].

Conflicting reports have led to two distinct and opposite recommendations (treatment modalities) on a surgical intervention following UTT: detorsion and preservation of the ipsilateral testis, or ipsilateral orchiectomy to preserve contralateral fertility [10].

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The aim of the present study

Therefore, the aim of the present study was to detect the microscopic changes in the contralateral testis and epididymis following corrective detorsion and following orchiectomy. It was also aimed to compare these changes and to determine which of the two procedures better preserves the testicular structure.

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Materials and methods

Thirty young adult male albino rats (2–3 months old) weighing 100–150 g were used in this study. They were housed in wire mesh cages and were provided free access to a balanced diet and water. They were divided into three groups (10 animals each).

Group I, Control group, included animals that were subjected to a sham operation. Their testes were exposed and replaced in the scrotum with orchiopexy.

Group II included animals that were subjected to left testicular torsion for 2 h. Then, the animals were subjected to ipsilateral detorsion, followed by a 1-week recovery period.

Group III: The animals were subjected to left testicular torsion for 2 h as in group II. Then, the animals were subjected to left testicular orchiectomy, followed by a 1-week recovery period.

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The surgical operation

The operation was carried out according to the procedure described by Cosentino et al. [11]. Twenty animals were anesthetized with sodium thiopental (40 mg/kg intraperitoneally) [12]. The skin of the scrotum was sterilized by tincture iodine. The left testis was exposed through a longitudinal scrotal incision and subjected to 720° of spermatic cord torsion for 2 h. The testis was replaced into the scrotum with repeated instillation of saline to prevent dryness of the testis. Then, it was fixed in place both medially and laterally using a 6-0 silk suture and the scrotum was closed by wound clips. After 2 h, under ether anesthesia, half of the animals underwent detorsion of ipsilateral (left) testis with orchiopexy (group II). The other half underwent spermatic cord ligation and complete excision of the left testis (ipsilateral orchiectomy) (group III). The scrotal skin was closed with 3-0 silk after homeostasis and local application of an antibiotic.

At the end of the experiment (after 1 week), the animals were sacrificed under light ether anesthesia. The right testes and epididymi from each animal were dissected out and were processed as follows:

For histological examination, testis and epididymis specimens were fixed in 10% formol saline, dehydrated, cleared, and embedded in paraffin. Paraffin sections (5 μm thick) were cut and then stained by H&E.

For transmission electron microscopic examination, specimens from the testis were fixed in a 4% glutaraldehyde solution. Semithin sections (1 μm thick) were prepared and stained with toluidine blue. Ultrathin sections were cut and examined using JEM- 1010 (Joel, Tokyo, Japan) at the Mycology and Biotechnology Unit, Al Azhar University, Cairo, Egypt.

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Morphometric and statistical study

The mean cross-sectional area and the mean spermatogenic height of the seminiferous tubules (SNTs) were measured. Five sections were analyzed for each animal. Five readings from each section were measured. The mean for each animal was calculated. The data were further analyzed using Student t-test and were considered significant when P < 0.05 (n=5).

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Results

Mortality

Three animals from group II and two animals from group III died within 24 h of the operation. They were excluded from the study.

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Naked eye examination

Following spermatic cord torsion, the testes became swollen, congested, and cyanosed within a few minutes. After detorsion (in group II), the color of the testes turned red but the testes were still swollen.

Examination of H&E-stained and toluidine blue-stained sections of the testis in the control group (group I) showed that the testis was formed of a large number of closely packed SNTs with regular outlines (Fig. 1).

Figure 1

Figure 1

The SNTs were surrounded by a thin regular basement membrane that was surrounded by myoid cells with flat nuclei. The tubules were lined by stratified epithelium that consisted of spermatogenic cells and Sertoli cells. Sertoli cells were observed at intervals between spermatogenic cells, detected by their large triangular or ovoid vesicular nuclei with prominent nucleoli and resting on their basement membrane (Figs 2 and 3).

Figure 2

Figure 2

Figure 3

Figure 3

Spermatogenic cells included spermatogonia, primary and secondary spermatocytes, spermatids, and finally mature sperm. Spermatogonia were small dome-shaped cells resting on the basement membranes. Primary spermatocytes appeared as the largest spermatogenic cells and were commonly observed in the sections. Their nuclei showed chromosomes in various stages of coiling. Secondary spermatocytes were small cells and rarely detected. Early spermatids appeared as small rounded cells with rounded central vesicular nuclei situated near the lumen. Late spermatids were detected with their elongated curved nuclei attached by their heads to the Sertoli cells (Figs 2 and 3).

The interstitial space between the SNTs was formed of a moderate amount of loose vascular connective tissue (Fig. 1). It contained groups of pale-stained interstitial cells of Leydig (ICL). The Leydig cells showed vesicular nuclei and a vacuolated cytoplasm (Figs 1, 3, and inset).

Examination of H&E-stained and toluidine blue-stained sections of the testis in group II indicated distortion of the SNTs with loss of the normal architecture. The spermatogenic cells were disorganized and separated from the underlying thin basement membranes, which were interrupted and ill defined in some tubules. Areas of cellular loss with multiple intercellular vacuoles were also observed in between the spermatogenic cells (Figs 4–6).

Figure 4

Figure 4

Figure 5

Figure 5

Figure 6

Figure 6

Most of the spermatogenic cells appeared small and degenerated, with loss of their normal arrangement. Spermatogonia appeared detached from the basement membrane and discontinuous in some tubules (Figs 5 and 6). Primary spermatocytes were small and many of them showed small darkly stained pyknotic nuclei (Figs 5 and 6). The lumina of the tubules contained acidophilic necrotic material and sloughed germ cells. with the absence of sperm in most of them (Figs 4 and 6).

Many multinucleated giant cells were detected in some SNTs and were surrounded by wide spaces. They showed four to nine nuclei and an acidophilic cytoplasm (Figs 4 and 7, inset).

Figure 7

Figure 7

Some SNTs were lined by a few layers formed of spermatogonia, primary spermatocytes, and Sertoli cells. The Sertoli cells were observed resting on the basement membrane and contained many lipid droplets. Many degenerated sloughed spermatogenic cells were also observed in their lumena (Fig. 8).

Figure 8

Figure 8

The interstitial spaces in between the tubules appeared wide and hypercellular. They showed acidophilic exudates, congested blood vessels, and an apparent increase in the number of ICL along with other mononuclear cellular infiltration (Figs 4, 5, and 9). The interstitial cells showed a vacuolated acidophilic cytoplasm and vesicular nuclei (Fig. 9a). ICL were also surrounded by necrotic materials and remnants of cells (Fig. 9b).

Figure 9

Figure 9

In sections of group III, most of the SNTs appeared lined by several layers of spermatogenic cells. Some SNTs showed sperm in their lumena (Fig. 10). However, a few of them were lined by few layers of spermatogenic cells and showed the absence of sperm. The cells appeared more organized and rested on a continuous basement membrane (Figs 10 and 11).

Figure 10

Figure 10

Figure 11

Figure 11

Spermatogonia and Sertoli cells were detected on the basement membranes, followed by primary spermatocytes, and early and late spermatids. Some of the tubules showed the appearance of the sperm (Figs 11 and 12).

Figure 12

Figure 12

The interstitial space was formed of loose vascular connective tissue and contained small groups of ICL (Figs 10 and 12).

The epididymis in the control group was formed of many tubules surrounded by a basement membrane, a thin layer of smooth muscle fibers, and connective tissue. The tubules were lined by pseudostratified ciliated columnar epithelium. The lumina of the tubules contained many sperm (Fig. 13a).

Figure 13

Figure 13

Sections of the epididymis in group II showed that the tubules were lined by apparently shorter epithelium than the control group. The tubules were also surrounded by wide spaces of loose connective tissue. These spaces contained acidophilic exudates and necrotic material. The lumina of the tubules were filled with remnants of cells, fragments of acidophilic cytoplasm, and exudates. Sperm were not detected in the lumina (Fig. 13b).

The epididymis in group III showed a picture similar to that of the control group. The connective tissue between the tubules was minimal and lumina of the tubules showed many sperm (Fig. 13c).

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Electron microscopic results

In the control group, spermatogonia were detected on the basal lamina and were partially covered by Sertoli cells. The spermatogonium cell body appeared dome-shaped or oval. The nucleus showed clumps of heterochromatin closely attached to the nuclear membrane. The cytoplasm was moderately electron dense. A few mitochondria, smooth endoplasmic reticulum, and free ribosomes were observed (Fig. 14).

Figure 14

Figure 14

Primary spermatocytes showed rounded nuclei of moderate electron density with dispersed heterochromatin. Synaptonemal complexes were detected in some of their nuclei. The cytoplasm showed Golgi complexes and many randomly arranged mitochondria (Fig. 15).

Early spermatids appeared as small spherical cells with round nuclei with finely granulofilamentous chromatin. Early spermatids were characterized by a peripheral arrangement of mitochondria and the presence of chromatoid bodies (Fig. 16). Cap formation could be detected by thickening of part of the nuclear membrane in some of them (Fig. 16).

Figure 15

Figure 15

The principal pieces of forming sperm appeared to have a central flagellum surrounded by nine coarse fibers. The end pieces show only nine coarse fibers covered by the cell membrane (Fig. 16 and inset).

Figure 16

Figure 16

Sertoli cells were found resting directly on the basement membrane. The nucleus was large, ovoid with infoldings of the nuclear membrane, and with a prominent central nucleolus. Mitochondria of variable sizes were found in the cytoplasm together with smooth endoplasmic reticulum. Large lipid droplets could be detected (Fig. 17). Myoid cells could also be observed surrounding the tubules (Fig. 17).

Figure 17

Figure 17

In the interstitial tissue between the SNTs, groups of interstitial cells of Leydig could be observed. They were rounded cells with cytoplasmic vacuoles, smooth endoplasmic reticulum, and several mitochondria (Fig. 18). In the interstitial tissue also, fibroblasts and some collagen fibers could be detected (Fig. 18).

Figure 18

Figure 18

In group II, the spermatogenic cells appeared irregular and their cytoplasm contained many vacuoles of variable sizes (Fig. 19). Some of the spermatogenic cells showed eccentric nuclei with finely granular chromatin (Fig. 19), whereas others showed indentation and compression of their nuclei and distorsion of the nearby cells by the huge vacuoles (Fig. 20). Cellular debris could be detected in the lumen (Fig. 19).

Figure 19

Figure 19

Figure 20

Figure 20

Early spermatids appeared irregular with small eccentric nuclei and showed many vacuoles. Disruption of their cell membrane was also observed. An apparent decrease in mitochondria was observed as compared with the control group (Figs 19 and 21). In the adluminal region of the SNT, many irregular cytoplasmic remnants containing vacuoles could be observed and forming multinucleated giant cells were also detected, containing from four to nine nuclei (Fig. 22).

Figure 21

Figure 21

Figure 22

Figure 22

Enlarged Leydig cells could also be observed in the interstitial tissue. They contained many vacuoles and electron-dense mitochondria. Some of them showed a disrupted cell membrane (Fig. 23).

Figure 23

Figure 23

Group III showed many layers of spermatogenic cells similar to that of the control. The primary spermatocytes showed dispersed heterochromatin within the nucleus. The cytoplasm showed a prominent Golgi apparatus and many mitochondria. The early spermatids showed peripherally situated mitochondria, chromatoid bodies, and acrosomal vesicles (Fig. 24). In some tubules, the early spermatids showed a moderately electron-dense cytoplasm with many vacuoles and an apparent decrease in the number of mitochondria. Cytoplasmic bridges could be detected between the cells (Fig. 25). Sertoli cells appeared more or less similar to those of the control group (Fig. 26).

Figure 24

Figure 24

Figure 25

Figure 25

Figure 26

Figure 26

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Statistical results

In group II (torsion detorsion group), the SNTs showed a significant decrease in the mean surface area of the SNTs and the mean spermatogenic height as compared with those of the control group (P < 0.05). However, group III (orchiectomy group) showed a nonsignificant change as compared with the control group I (Table 1).

Table 1

Table 1

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Discussion

Acute scrotum is a clinical syndrome mainly caused by torsion of the spermatic cord that constitutes a surgical emergency affecting newborns, children, and adolescents. This syndrome often leads to infertility because the ipsilateral (torted) and contralateral (not torted) testis are affected, an outcome that makes surgical intervention mandatory [10].

The present study observed many structural alterations in the contralateral testis 2 h following unilateral testicular torsion detorsion (UTD). In this study, sloughing and exfoliation of the germ cells in the lumina of the tubules were observed. In addition, large vacuoles were detected in between the spermatogenic epithelium. Similarly, many reports have shown that UTD results in contralateral testicular damage. This damage included an uneven distribution of the SNTs, interstitial edema, markedly reduced numbers of spermatogenic cells up to the absence of germ cells, and replacement of tubules by hyaline material in addition to apoptosis and sloughing of germ cells [6,8,13–17].

The exfoliation of the germ cells could be because of a primary effect on the cell-to-cell junctions between Sertoli and germ cells [15]. Moreover, the spaces and vacuoles detected in between the spermatogenic epithelium might be because of the exfoliation and the sloughing of germ cells [13].

The mechanism of contralateral testicular damage after UTD remains controversial. Multiple factors contribute toward the injury of the contralateral testis after UTD. The main pathophysiology of testicular torsion detorsion is I/R injury of the testis [18].

Accordingly, different authors have suggested a role of blood supply in the contralateral testicular affection, although the results have been contradictory. Many authors have reported that UTT causes a decrease in the contralateral testicular blood flow and hypoxia, which may lead to contralateral degeneration of germ cells and testicular damage [8,15]. However, other authors have reported increased, rather than reduced, blood perfusion after UTD in the contralateral testis [19,20]. The present results were in agreement with those of the increased blood perfusion studies as detected by the congested blood vessels.

The testis is controlled by the visceral sympathetic nerves [21], and testicular parenchyma shows very rich innervation, distributed mainly to the blood vessels [22]. The visceral sympathetic nerves can be activated after UTT and may cause an increase in the blood perfusion in the contralateral testis [19].

The SNTs are avascular and yet very metabolically active. The SNTs depend on the transport of oxygen and nutrients from the interstitial vasculature and require a regular blood flow to maintain normal spermatogenesis. Therefore, they are susceptible to alterations in blood flow. Moreover, PO2 is dependent on blood flow and disturbances in blood flow may easily alter the amount of oxygen available for critical metabolic processes in spermatogenesis [23].

Reperfusion time appears to be a determinant of contralateral testicular damage because of the consequent oxidative insult that accompanies the increase in ROS following I/R [10]. Furthermore, Akcora et al., in their experimental study, concluded that gradual detorsion in two steps decreased the degree of testicular reperfusion injury in rats. This was detected by significant decreased superoxide dismutase and glutathione peroxidase activities in the sudden detorsion group as compared with the gradual detorsion group as well as preservation of the structure of the testis [24].

Testicular torsion caused loss of spermatogenesis and a significant increase in germ cell apoptosis arising from a significant increase in the proapoptotic molecules and intratesticular ROS concomitant with reperfusion [25]. When ROS production exceeds the capacity of the defense mechanisms, cell damage occurs as mammalian testes are highly sensitive to oxidative free radical damage [5,26].

Moreover, upon reperfusion of the tissue, oxygen becomes available, resulting in the generation of a huge amount of free radicals that react with the lipids present in the cell membrane and mitochondrial membrane, leading to the disruption of the integrity of the cell and damage to the cell membrane. Sperm are highly sensitive to oxidative stress and particularly to lipid peroxidation because of their high content of polyunsaturated fatty acids in the plasma membrane [27,28].

Oxidative stress arises with the recruitment of neutrophils, which secrete inflammatory cytokines such as tumor necrosis factor-α, interleukin-1β, and interleukin-8. The invading neutrophils may also secrete factors that induce Sertoli cells to secrete FasL [29]. Fas receptors are present on the germ cell membrane. FasL binding initiates the intracellular ‘death domain’ pathway, which leads to DNA degradation, thus causing germ cell death [30].

By electron microscopic examination, the present results showed that the primary spermatocytes and the spermatids were principally affected. The abnormalities included cytoplasmic vacuoles, a decrease in mitochondria, and irregular nuclei. Similar results have been obtained in previous studies [31]. It has been reported that spermatogonia, capillary endothelium, connective tissue, and peritubular fibroblasts are rarely involved. Trauma to the blood–testis barrier initiated by testicular torsion induces the release of apoptotic-activating factors (cytokines), which subsequently cause extensive apoptosis in the germinal epithelium of the contralateral testis [32].

In the present work, many multinucleated giant cells were observed inside the tubules. A similar observation has been made in a previous study [13]. Other authors have reported testicular multinucleated giant cells as a degenerative syndrome resulting from the inability of tetraploid primary spermatocytes to complete meiotic division; thus, maturation arrested at the spermatid stage of development [33]. Giant cells may also be formed as a result of the fusion of spermatids because of alterations in the intercellular bridges [34]. Moreover, it has been suggested that multinucleated giant cells could be aggregates of degenerated spermatocytes and spermatids that were often sloughed into the lumen of the SNTs [33].

Other studies have reported that histopathologic testicular damage and humoral and cellular immune responses occur simultaneously in the contralateral testis after UTD. They suggested the involvement of an immunologic mechanism in the induction of the lesion in the contralateral testis [16]. Other theories proposed included autoimmunity and the release of acrosomal enzyme [8].

The results of the present study showed that interstitial spaces were wide and hypercellular with congested blood vessels. There was an apparent increase in the number of Leydig cells along with other mononuclear cellular infiltration. These results were in agreement with those of a previous study [35]. The authors found clusters of Leydig cells surrounded by many cells such as plasma cells and macrophages and increased fibroblasts in the interstitium.

The vacuolation and the apparent increase in the number of interstitial cells that was observed in the present work might be attributed to increased activity of Leydig cells. It has been reported that Leydig cells normally release their hormones into the interstitium, from which it diffuses to the tubules to exert their local effect on spermatogenesis and into blood and lymphatic vessels to exert their systemic effect. The SNTs feed back to inhibit Leydig cells. Therefore, any local damage to SNTs appears to reduce this inhibitory effect and induces hypertrophy and increased activity of Leydig cells [36].

In addition, I/R injury resembles an inflammatory response, resulting in the activation of endothelial cells and subsequent leukocyte margination, followed by diapedesis to the interstitium of the testis, increasing the number of cells in the interstitium [25].

In the present study, the epididymis following UTD showed that contralateral epididymal tubules were full of exudates, necrotic material, degenerated cells, and absent sperm. The tubules were surrounded by wide connective tissue spaces containing inflammatory cells, exudates, necrotic material, and congested blood vessels. The structural changes in the epididymis could be a consequence of the changes detected in the SNTs. As the lumena of the SNTs were filled with necrotic material, exudates with absence of sperms, it is also expected that the epididymal tubule show the same content.

In the present work, in the contralateral testis after testicular torsion and orchiectomy, the spermatogenic cells lining most of the SNTs were organized and rested on their surrounding basement membranes. The lumina of the tubules contained late spermatids with their long tails.

These results were in agreement with the results of a previous study. The authors reported that the structural changes in the contralateral testis in the torsion/detorsion group were significantly more (58.6%) than those of the torsion/orchiectomy group (48.0%) [13].

Moreover, many authors have suggested that orchiectomy had a prophylactic value and maintained fertility more than detorsion after testicular torsion in the contralateral testis [11,37].

An explanation for this could be that after the detorsion procedure, reperfusion not only increased blood flow but also increased the presence of oxygen free radicals, which caused cellular damage through lipid peroxidation [38]. It has been reported that the tissue superoxide dismutase level decreased more in animals that underwent detorsion procedures than in orchiectomized animals [39].

In contrast, in a recent clinical study, it was concluded that detorsion with orchiopexy yields better testicular function than orchiectomy in the short term. This was detected by the high levels of testosterone and serum inhibin B levels [40].

Moreover, Romeo et al. carried out a prospective study evaluating patients 5 years following testicular torsion. They reported that hormonal testicular function could be compromised after testicular torsion, although the type of surgery (orchiectomy or detorsion) did not seem to alter the effect of this I/R injury [41].

There is a possibility of an immunologic mechanism that damages the contralateral testis. Testicular torsion results in exposure of the antigenic stimulation, thus increasing the immunologic mechanisms. Therefore, removal of the torted testis would tend to protect against the development of contralateral testicular damage. Furthermore, the return of blood flow to a testis that was already damaged (detorsion) might increase the stimulation of a presumed immune-mediated attack on the contralateral testis [42].

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Conclusion

The present results showed that orchiectomy following testicular torsion better preserved the structure of the contralateral testis and epididymis as compared with detorsion. Taking into consideration the current methodology (study plan), it cannot be generalized that orchiectomy is the favorable choice. Many factors may have played a role in the outcome of the study: the duration of the experiment (1 week), the duration of torsion (2 h), the degree of torsion (720°), the species (rat), and the sudden detorsion. Therefore, further studies are required to analyze each of these factors to obtain a more specific and detailed protocol as to when to choose orchiectomy and when to choose detorsion.

Table

Table

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Acknowledgements

Conflicts of interest

There is no conflict of interest to declare.

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Keywords:

contralateral testis; detorsion; orchiectomy; testicular torsion.

© 2012 The Egyptian Journal of Histology