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Testicular torsion in adolescents

Shaeer, Kamal Z.; Shaeer, Osama K.; Ragab, Mohamed W.

doi: 10.1097/01.XHA.0000496449.53293.3d
Review articles
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Testicular torsion is one of the common causes of acute scrotum in adolescents. Early diagnosis and proper surgical management is crucial for testicular salvage. Although testicular torsion was first described in 1840, it is one of the most common reasons for malpractice lawsuits among adolescent boys. This review article aimed to highlight all clinical, diagnostic, and management aspects of testicular torsion, emphasizing on recent updates and experimental studies in that field. We reviewed already published articles in this context using PubMed, Medical Subject Headings database, Cochrane Central Register of Controlled Trials, and Google Scholar until April 2015. We used testicular torsion and acute scrotum as keywords. Most studies on this subject were correlated to management, differential diagnosis, surgical interventions, and experimental studies in the field of minimizing ischemia–reperfusion injury. Recent publications focused on providing highly sensitive and specific diagnostic methods and on improving the testicular salvage rate.

Department of Andrology, Faculty of Medicine, Cairo University, Cairo, Egypt

Correspondence to Mohamed W. Ragab, MSc, Department of Andrology, Faculty of Medicine, Cairo University, Cairo 12622, Egypt Tel: +20 127 990 9997; e-mail: dr.wa2el@gmail.com

Received October 25, 2015

Accepted August 14, 2016

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Introduction

Historical background

In Greek mythology, it was believed that Gods would shoot young healthy men with arrows, which would cause pain, followed by testicular atrophy. The condition of sudden pain, detected by palpation as a tender scrotal swelling and progression to testicular atrophy, was highlighted early in history as torsion of the spermatic cord 1.

In 1776, Hunter mentioned what can be considered a case of left testicular torsion in an 18-year-old man who presented with the typical clinical presentation of acute scrotum. After a few weeks the testis atrophied ‘to the size of a horse bean.’ One year later, torsion occurred on the right side, followed by ipsilateral atrophy 2. The first reported case of torsion of an undescended testis was published in 1840 by the French psychiatrist Louis Delasiauve 3. Lauenstein 4 was the first to publish original and schematic illustrations of testicular torsion and also the first to classify it in 1894.

In 1922, torsion of the testicular appendix was described by Colt 5. Further, the first illustration was made by Mouchet 6.

Surprisingly, with such a long history of identification and development of different diagnostic technologies, testicular torsion is the third most common reason for malpractice lawsuits in adolescent boys in the USA 7.

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Epidemiology

Incidence of testicular torsion is bimodal, with the first peak occurring in adolescent boys aged 12–18 years and a second less common peak being in the first year of life 8. However, it can be seen in any age group. Intravaginal torsion has been reported in as young as a newborn baby and in as old as a 77-year-old man. Sixty-two percent of cases occur in patients aged 12–18 years and 89% below the age of 25 years 9. It is estimated that 1/4000 men under the age of 25 will have torsion of the testis 10.

Testicular torsion is the cause of 16–39.5% of cases of acute scrotum in childhood 11. Testicular torsion is the most common cause of acute scrotum in the first year of life (83%). From the age of 3–13 years, the most common cause is torsion of testicular appendages. In the male population over 17 years, epididymitis is the most common cause of acute scrotum (75%) 12.

Regarding torsion of appendages, about 82% of cases occur between the ages of 7 and 14 years. However, it has been reported in the first to fifth decade of life 13–15. The testicular appendix is involved in 92% of cases, the epididymal appendix in 7%, the paradidymis in 0.6%, and the vas aberrans in 0.3% of cases 16.

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Pathophysiology

According to its relation to the tunica vaginalis, testicular torsion is classified into two types. The first type, which is intravaginal torsion, occurs within the tunica vaginalis and is the most common type. The second type of testicular torsion is termed extravaginal torsion. It occurs in newborns when the testis and its gubernaculum can rotate freely in the scrotum 17.

Intravaginal torsion requires an anatomical predisposition for torsion. Torsion is triggered by an initiating force. Torsion occurs in the direction of the internal rotation in 71–100% of cases 18,19. The degree of rotation ranges from 180° to 1440° 14. A single study showed a significantly higher degree of rotation (mean=585°) in patients aged 21 years or more compared with that in patients younger than 21 years of age (mean=431°) 20. This rotation compromises the blood flow of the testis and obstructs the veins of the cord first on account of their thinner walls. Bound by the connective tissue coverings of the spermatic cord, pressure within the congested veins increases pressure within the cord, ending in obstruction of arterial inflow, even if the torsion is unable to occlude the artery directly 21. Direct arterial occlusion requires multiple twists 22.Testicular torsion induces ischemic injury, and torsion repair induces an ischemia–reperfusion (I/R) injury that disrupts the testicular spermatogenic and endocrinal functions by different mechanisms including induction of apoptosis, activation of neutrophils, upregulation of endothelial cell adhesion molecules and inflammatory cytokines, release of intracellular Ca2+, and generation of reactive oxygen species (ROS) 23.

Testicular salvage rate depends on the degree of rotation of the spermatic cord and the duration of spermatic cord torsion. Kolettis et al.24 found in a canine model study that 90° rotation of the spermatic cord led to a pathological picture of necrosis within 7 days. Similar findings were obtained by 360° rotation within 12–24 h. A 1440° rotation of the cord resulted in complete necrosis of the testicle within 2 h.

Early management of testicular torsion improves the salvage rate of the affected testis. In a large single institution series that involved 624 cases, viability at exploration in relation to 0-6, 7-12 and >48 hours of spermatic cord torsion was found to be 98%, 90% and 8% respectively 9. In a meta-analysis that involved 1140 patients from 22 reports and another one that involved 535 patients in eight series, Visser and Heyns 26 similar results were found.

The urgent versus elective management of cases of delayed presentation of torsion is a debatable point. These reports, as well as other reports 27–29, provide strong evidence against the misconception that testicular torsion presenting after 6 h should not be treated as an emergency as it is not salvageable.

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Anatomical predisposition for testicular torsion

Intravaginal testicular torsion is predisposed to the presence of bell-clapper deformity, spiral arrangement, and low insertion of the cremasteric muscle and abnormal junction between the epididymis and the testis, forming a mesorchium 13. Bell-clapper deformity, which is proximal extension of the tunica vaginalis around the spermatic cord, is found in 12% of autopsies, and is bilateral in 66% of cases, suggesting that it is a common deformity in humans and its prevalence is more than torsion 30. Against the myth that bell-clapper deformity is present invariably in intravaginal testicular torsion, bell-clapper deformity was found in 71–75% of cases of intravaginal testicular torsion 18,31. Testicular torsion occurs ten times more in patients with undescended testes 14. Before 1952, 60% of all cases of torsion were seen along with cryptorchidism. These numbers decreased sharply because of routine orchiopexy during surgical repair of undescended testis 1. Extravaginal torsion, which is found in neonates, occurs because of free mobility of the neonatal tunica vaginalis and its contents inside the scrotum 14,32 (Figs 1 and 2).

Figure 1

Figure 1

Figure 2

Figure 2

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Initiating force

Cremasteric spasm, which holds the testis in the torsed position, was found to be associated with trauma, vigorous exercise, and cold weather, and to occur even during sleep 33. The peripubertal increase in testicular size relative to the spermatic cord may contribute to torsion by adding a greater momentum to any twisting action 14. The same mechanism may explain the occurrence of testicular torsion in several reported cases of patients on human chorionic gonadotrophin therapy 34,35.

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Genetic background of testicular torsion

A genetic basis for testicular torsion has been suspected after numerous published reports of familial testicular torsion appeared 36–39.

A meta-analysis showed that up to 10% of testicular torsion patients have a positive family history in a first-degree relative, with high incidence of bilateral testicular torsion in familial cases (37%) 39.

INSL3 hormone and its receptor RXLF2 have been suggested as candidate genes for testicular torsion. INSL3 is a hormone secreted by Leydig cells and regulates the growth and differentiation of the gubernaculum; thus, it mediates intra-abdominal testicular descent 40. INSL3 knock-out mice invariably manifest with intra-abdominal bilateral cryptorchidism with subsequent heat-induced atrophy of the testes in adulthood, and spontaneous testicular torsion, which occurred peripubertally in most of the cases 41.

In contrast, in a study that involved 39 male patients with surgically confirmed testicular torsion (11 neonatal, 21 peripubertal, and seven pubertal), a positive family history of torsion was present in 29% of neonatal and 33% of peripubertal cases. Nonsignificant mutations in INSL3 or RXFP2 could be linked to testicular torsion 42. However, this ligand-receptor signaling system may be still linked to testicular torsion by another level of regulation.

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Clinical features

Testicular torsion should be suspected in neonates and peripubertal boys presenting with acute scrotum; torsion of a testicular appendage is more common in prepubertal boys, and epididymitis most often develops in postpubertal boys 43.

Testicular torsion pain is characterized by being acute and severe, and begins to diminish after 6 h 44. Gradual moderate pain is more suggestive of epididymitis or appendiceal torsion 43. Abdominal pain may be the presenting symptom in 5–25% of patients 9,44. Nausea and vomiting may be present in 26–60% of testicular torsion cases. Nausea has a positive predictive value of 96% and vomiting 98% for torsion, but both have lower sensitivity 16,45. Urinary complaints are not pathognomonic for genital tract infection and should not be used to exclude testicular torsion. Urinary symptoms are present in 5–7% of patients with testicular torsion. The symptoms are typically slight frequency and dysuria. Interestingly, urinary complaints are also found in 7% of cases with acute epididymitis 9,31. History of previous episodes of similar pain (prophetic pain) that resolved spontaneously is present in 11–47% of patients, suggesting intermittent torsion with spontaneous detorsion 16,31.

Cremasteric reflex is a superficial skin reflex mediated by ilioinguinal and genitofemoral nerve roots (L1–L2). It is elicited by stroking the medial upper thigh, and a positive reflex results in contraction of cremastric muscle and elevation of the ipsilateral testis. A point of controversy is that cremastric reflex is absent in 100% in the torsed side according to one report 46. Several reports confirmed torsion of the testis with a normal cremasteric reflex 47,48 with a sensitivity of 60% and specificity of 67% for torsion of the testis 35. A drawn-up testis is present in 26–80% of cases of testicular torsion 16,35. Between 25 and 90% of patients with torsion will have an abnormal lie of the contralateral testis (Angell’s sign). Fever is present in 8–41% of cases with testicular torsion and has a bad prognosis regarding testicular viability 9,49,50. Scrotal edema and induration also denote bad prognosis and are associated with torsion for more than 12 h 51,52.

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Diagnostic imaging

Although some cases of testicular torsion may have pathognomonic history or clinical examination findings, color Doppler ultrasound (CDU) is still the first-line radiological diagnostic tool for a patient presenting with acute scrotum to exclude testicular torsion 53. The most important CDU finding is absence of any detectable perfusion of the affected testis 10. Relying on history and clinical examination alone is inaccurate as there is a high probability of misdiagnosis. According to a retrospective review of 204 patients presenting with acute scrotum, relaying on history and clinical examination alone resulted in misdiagnosis of five cases of testicular torsion and the preoperative diagnosis was accurate only in 80% of operated cases 54. CDU is currently the diagnostic tool of choice in suspected cases, as it is easy to perform, is readily available, and provides information that could exclude other conditions such as epididymo-orchitis. However, it is an operator-dependent procedure, and sometimes normal blood flow is not detected in small-sized untorsed testes. The presence of blood flow does not exclude torsion 55–57. Testicular salvage after detorsion can be predicted by color Doppler ultrasonography; parenchymal heterogeneity of the testicular echotexture and absence of testicular blood flow indicate late torsion and testicular nonviability 58.

Lam et al.59 reported a sensitivity of 69.2%, specificity of 100%, positive predictive value of 100%, and negative predictive value of 97.5% in the diagnosis of testicular torsion by CDU. In 323 patients who had negative ultrasound findings, 29 were surgically explored on a clinical basis. Four of these 323 patients (1.2%) were diagnosed intraoperatively as testicular torsion 59.

Lower diagnostic values were reported by Kalfa et al.60, who published a multicenter study that involved 208 patients with testicular torsion proven by surgical exploration. Testicular torsion was misdiagnosed by CDU in 50 cases (24%). Kalfa et al.60 compared these results with the results of high-resolution ultrasonography in 919 patients aged 1–18 years (mean=9) for the direct visualization of the torsion of the spermatic cord as a spiral twist of the cord resembling snail shell or ‘whirlpool sign’. Testicular torsion was diagnosed in 199 of 208 patients (96%). Testicular torsion was excluded by finding linear cord for all other causes of acute scrotum (711 patients) with a specificity of 99% 60,61.

Near-infrared spectroscopy is a more recent noninvasive technology that is based on utilizing infrared light to obtain transcutaneous monitoring of deep tissue oxygen saturation. In its pilot study for using this technology in the assessment of acute scrotum, near-infrared spectroscopy identified all surgically confirmed cases of testicular torsion 62.

Other diagnostic modalities such as scintigraphy 63–66 and scrotal dynamic contrast-enhanced subtraction MRI 67 may be used when testicular torsion is unlikely but cannot be excluded. Scintigraphy is carried out using technetium-99m to assess testicular perfusion. It has been used since 1973 63,64. Testicular torsion is represented by a cold spot of no isotope uptake with a hot perimeter of relatively increased uptake (halo sign) 64. A similar picture may be present in hematoma, abscess, and tumors of the testis. However, those tools are not always available and may cause delay for emergency intervention 54.

On the laboratory level, a recent animal model study suggested that plasma D-dimer level can be used as a diagnostic marker of testicular torsion 68.

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Differential diagnosis

In any case presenting with acute scrotum, testicular torsion should be suspected and excluded. In the first year of life, testicular torsion is considered the most common cause of acute scrotum (83%). However, some studies have found that epididymo-orchitis is present in 69% of cases and testicular torsion in 31% of cases of acute scrotum in the first year of life 69. Among male patients aged 3–13 years, the most common cause of acute scrotum is torsion of the testicular appendages. After the age of 17 years, epididymitis is considered the most common cause 12. Differential diagnosis of acute scrotum is summarized in Table 1.

Table 1

Table 1

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Management of testicular torsion

Immediate surgical exploration is indicated in all patients who presented with testicular torsion within 24 h of symptom onset. As mentioned before, testicular salvage rates decrease with increased duration of testicular torsion. Early detorsion (duration of torsion<13 h) was found to preserve fertility 82. In patients with neglected testicular torsion (duration of torsion>24 h) semielective exploration is indicated. Immediate surgery is indicated in all cases of acute solitary testis 26,82,83. Torsion of the appendix testis is managed conservatively by anti-inflammatory and analgesics 43. Surgical exploration is preserved for equivocal cases 84.

Scrotal cooling was suggested before surgical exploration 12 as it was found to preserve the testicular function 85.

Exploration of both hemiscrotum contents can be performed through a single median raphe incision. When the torsed testis is obviously necrotic, it should be removed. Equivocal testes should be wrapped in warm moist saline gauze for 5–10 min and then reassessed for testicular viability. Viable testes are detorsed and fixed. Routinely, contralateral fixation should be done 86. Contralateral fixation could be done either by three nonabsorbable fixation or by dartos poche 87,88.

One study suggested that further testicular damage occurs after detorsion because of the so-called ‘testicular compartment syndrome’; increased intratesticular pressure against the tough tunica albuginea leads to decreased perfusion to the testis and further ischemic injury 89. Kutikov and colleagues proposed a novel technique to avoid ‘testicular compartment syndrome’ by making an incision over the tunica albuginea, in a similar manner to fasciotomy, with placement of a tunica vaginalis patch during detorsion. This should allow for edema to ensue without increasing the compartmental pressure 89–91.

Manual detorsion is a simple and organ-saving procedure that can be performed with or without anesthesia. It should initially be done by outwards (like opening book) rotation of the testis unless the pain increases, or if there is obvious resistance, in which case rotation to the opposite side should be tried. Success is defined as immediate relief from pain 92. It can be done under the guidance of CDU 19. It is considered a temporary measure; residual torsion is present in up to 28% of cases. However, this maneuver has up to 80% success rate 45,92.

In this context, obtaining consent from adults or parents of minors regarding misdiagnosis of testicular appendix torsion or epididymo-orchitis as testicular torsion or necessity of orchiectomy of delayed diagnosed torsed testis is of importance.

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Drugs used to minimize ischemia–reperfusion injury

Many recent publications have focused on minimizing testicular damage induced by I/R injury after testicular torsion. Germ cell apoptosis and DNA damage is mediated by several mechanisms such as neutrophil recruitment and release of ROS such as superoxide dismutase, glutathione peroxidase, and malondialdehyde. ROS scavengers have been hypothesized to have a protective effect against I/R injury following surgical correction of testicular torsion. However, all conducted studies were performed on a rat model 61,93.

Sildenafil, vardenafil, and taladafil, which are phosphodiestrase-5 inhibitors; were injected intraperitoneally after intiation of experimental testicular torsion. Testicular tissue levels of malondialdehyde and nitric oxide synthase expression were significantly lower and total testicular antioxidant levels were higher in rats given medication as compared with those that simply underwent torsion/detorsion 94–96. Rosuvastatin is an antihyperlipidemic drug with anti-inflammatory and tissue protective effects. In a single study, it was found that when rosuvastatin was injected intraperitoneally after intiation of testicular torsion, testicular microvascular perfusion was increased 97. The use of apocynin (NADPH oxidase inhibitor) was found to decrease free radical generation and increase antioxidant protective effects on testicular tissues against I/R injury in one study 98. Polyadenosine diphosphate-ribose polymerase inhibitors such as nicotinamide, 3-aminobenzamide, 1,5-dihydroxyisoquinoline, and 4-amino-1,8-naphthalimide were found to inhibit poly (ADP-ribose) polymerase, which is one of the enzymes that play a role in testicular damage caused by I/R 99. Thymoquinone is a phytochemical compound found in the plant Nigella sativa. Thymoquinone significantly reduces the apoptotic index, active-caspase 3, and Bax expression 93. Coenzyme Q10 is an oil-soluble vitamin-like substance that is present in eukaryotic cells, mainly in the mitochondria. It acts as an antioxidant and plays a role in the electron transport chain. The use of coenzyme Q10 before reperfusion resulted in significant decrease in products of testicular lipid peroxidation; inducible nitric oxide synthase and endothelial nitric oxide synthase decreased, leading to minimization of germ cell-specific apoptosis 100.

Other drugs that have been studied in rat models of testicular torsion and showed promising outcome include lycopene 101, ginkgo biloba 102, melatonin 103, N-acetylcysteine 104, and erythropoietin 105.

Local injection of mesenchymal stem cells has been investigated in the protection of testicular torsion-induced germ cell injury. In a study by Hsiao et al.106, local injections of mesenchymal stem cells from human orbital fat tissues n a rat model minimized torsion-induced germ cell apoptosis and oxidative stress compared with the control group.

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Future perspectives

Recognition of certain genetic defects that predispose to testicular torsion is important for therapeutic development, and prophylactic orchiopexy may be considered once those genes are discovered.

Advances in diagnostic technologies may also help to provide a highly specific and sensitive technology that could minimize unnecessary surgical exploration and misdiagnosed testicular torsion.

Several recent studies have shown promising effects of certain medications in minimizing I/R injury in rat models. Studies that test the efficacy and safety of these medications on humans should be among our priorities.

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Acknowledgements

Conflicts of interest

There are no conflicts of interest.

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References

1. Nöske HD, Kraus SW, Altinkilic BM, Weidner W. Historical milestones regarding torsion of the scrotal organs. J Urol 1998; 159:13–16.
2. Hunter J. Atreatise on the venereal disease. London, UK: G Nicol and J Johnson; 1810.
3. Delasiauve LJF. Late descent of the left testicle, misdiagnosed as strangulated hernia [in French]. Rev med franc et etrang 1840; 1:363–375.
4. Lauenstein C. Testicular torsion [in German]. Sammlung Klin Vortr 1894; 92:1.
5. Colt GH. Torsion of the hydatid of Morgagni. Brit J Surg 1922; 9:464.
6. Mouchet A. A variety of acute orchitis childhood which was found to be a twist of the hydatid of Morgagni [in French]. Presse Med 1923; 43:485.
7. Selbst SM, Friedman MJ, Singh SB. Epidemiology and etiology of malpractice lawsuits involving children in US emergency departments and urgent care centers. Pediatr Emerg Care 2005; 21:165–169.
8. Prater JM, Overdorf BS. Testicular torsion: a surgical emergency. Am Fam Physician 1991; 44:834–840.
9. Anderson JB, Williamson RC. Testicular torsion in Bristol: a 25-year review. Br J Surg 1988; 75:988–992.
10. Ringdahl E, Teague L. Testicular torsion. Am Fam Physician 2006; 74:1739–1743.
11. Marcozzi D, Suner S. The nontraumatic, acute scrotum. Emerg Med Clin North Am 2001; 19:547–568.
12. Lewis AG, Bukowski TP, Jarvis PD, Wacksman J, Sheldon CA. Evaluation of acute scrotum in the emergency department. J Pediatr Surg 1995; 30:277–281. discussion 281–282.
13. Jones P. Torsion of the testis and its appendages during childhood. Arch Dis Child 1962; 37:214–226.
14. Williamson RC. Torsion of the testis and allied conditions. Br J Surg 1976; 63:465–476.
15. Holland JM, Graham JB, Ignatoff JM. Conservative management of twisted testicular appendages. J Urol 1981; 125:213–214.
16. Skoglund RW, McRoberts JW, Ragde H. Torsion of the spermatic cord: a review of the literature and an analysis of 70 new cases. J Urol 1970; 104:604–607.
17. Backhouse KM. Embryology of testicular descent and maldescent. Urol Clin North Am 1982; 9:315–325.
18. Ransler CW 3rd, Allen TD. Torsion of the spermatic cord. Urol Clin North Am 1982; 9:245–250.
19. Garel L, Dubois J, Azzie G, Filiatrault D, Grignon A, Yazbeck S. Preoperative manual detorsion of the spermatic cord with Doppler ultrasound monitoring in patients with intravaginal acute testicular torsion. Pediatr Radiol 2000; 30:41–44.
20. Cummings JM, Boullier JA, Sekhon D, Bose K. Adult testicular torsion. J Urol 2002; 167:2109–2110.
21. Chen DC, Holder LE, Melloul M. Radionuclide scrotal imaging: further experience with 210 patients. Part I: anatomy, pathophysiology, and methods. J Nucl Med 1983; 24:735–742.
22. Cuckow PM, Frank JD. Torsion of the testis. BJU Int 2000; 86:349–353.
23. McCord JM. Oxygen-derived free radicals in postischemic tissue injury. N Engl J Med 1985; 312:159–163.
24. Kolettis PN, Stowe NT, Inman SR, Thomas AJ Jr. Acute spermatic cord torsion alters the microcirculation of the contralateral testis. J Urol 1996; 155:350–354.
25. Heyns CF, Visser AJ. Schill WB, Comhaire F, Hargreave T. Testicular torsion. Andrology for the clinician. Berlin; Heidelberg: Springer; 2006. 134–161.
    26. Visser AJ, Heyns CF. Testicular function after torsion of the spermatic cord. BJU Int 2003; 92:200–203.
    27. Klingerman JJ, Nourse MH. Torsion of the spermatic cord. JAMA 1967; 200:673–675.
    28. Arce JD, Cortés M, Vargas JC. Sonographic diagnosis of acute spermatic cord torsion. Rotation of the cord: a key to the diagnosis. Pediatr Radiol 2002; 32:485–491.
    29. Hegarty PK, Walsh E, Corcoran MO. Exploration of the acute scrotum: a retrospective analysis of 100 consecutive cases. Ir J Med Sci 2001; 170:181–182.
    30. Caesar RE, Kaplan GW. Incidence of the bell-clapper deformity in an autopsy series. Urology 1994; 44:114–116.
    31. Cass AS, Cass BP, Veeraraghavan K. Immediate exploration of the unilateral acute scrotum in young male subjects. J Urol 1980; 124:829–832.
    32. Al-Salem AH. Intra-uterine testicular torsion: early diagnosis and treatment. BJU Int 1999; 83:1023–1025.
    33. Williamson RC. The continuing conundrum of testicular torsion. Br J Surg 1985; 72:509–510.
    34. Sawchuk T, Costabile RA, Howards SS, Rodgers BM. Spermatic cord torsion in an infant receiving human chorionic gonadotropin. J Urol 1993; 150:1212–1213.
    35. Van Glabeke E, Khairouni A, Larroquet M, Audry G, Gruner M. Acute scrotal pain in children: results of 543 surgical explorations. Pediatr Surg Int 1999; 15:353–357.
    36. Cubillos J, Palmer JS, Friedman SC, Freyle J, Lowe FC, Palmer LS. Familial testicular torsion. J Urol 2011; 185 (Suppl):2469–2472.
    37. Gorbonos A, Cheng EY. Perinatal testicular torsion in siblings. J Pediatr Urol 2007; 3:514–515.
    38. Collins K, Broecker BH. Familial torsion of the spermatic cord. J Urol 1989; 141:128–129.
    39. Shteynshlyuger A, Yu J. Familial testicular torsion: a meta analysis suggests inheritance. J Pediatr Urol 2013; 9:683–690.
    40. Nef S, Parada LF. Cryptorchidism in mice mutant for Insl3. Nat Genet 1999; 22:295–299.
    41. Sozubir S, Barber T, Wang Y, Ahn C, Zhang S, Verma S, et al.. Loss of Insl3: a potential predisposing factor for testicular torsion. J Urol 2010; 183:2373–2379.
    42. Wang Y, Fina M, Zhang S, Taussig R, Baker LA. Screening for a genetic basis for testicular torsion: the insulin-3 (Insl3) and Lgr8 genes. J Urol 2008; 179:147.
    43. Galejs LE. Diagnosis and treatment of the acute scrotum. Am Fam Physician 1999; 59:817–824.
    44. Sparks JP. Torsion of the testis. Ann R Coll Surg Engl 1971; 49:77–91.
    45. Jefferson RH, Pérez LM, Joseph DB. Critical analysis of the clinical presentation of acute scrotum: a 9-year experience at a single institution. J Urol 1997; 158 (Pt 2):1198–1200.
    46. Rabinowitz R. The importance of the cremasteric reflex in acute scrotal swelling in children. J Urol 1984; 132:89–90.
    47. Blaivas M, Batts M, Lambert M. Ultrasonographic diagnosis of testicular torsion by emergency physicians. Am J Emerg Med 2000; 18:198–200.
    48. Beni-Israel T, Goldman M, Bar Chaim S, Kozer E. Clinical predictors for testicular torsion as seen in the pediatric ED. Am J Emerg Med 2010; 28:786–789.
    49. Kaplan GW, King LR. Acute scrotal swelling in children. J Urol 1970; 104:219–223.
    50. Parker RM, Robison JR. Anatomy and diagnosis of torsion of the testicle. J Urol 1971; 106:243–247.
    51. Angell JC. Torsion of the testicle. A plea for diagnosis. Lancet 1963; 1:19–21.
    52. Hemalatha V, Rickwood AM. The diagnosis and management of acute scrotal conditions in boys. Br J Urol 1981; 53:455–459.
    53. Baker LA, Sigman D, Mathews RI, Benson J, Docimo SG. An analysis of clinical outcomes using color Doppler testicular ultrasound for testicular torsion. Pediatrics 2000; 105 (Pt 1):604–607.
    54. Mushtaq I, Fung M, Glasson MJ. Retrospective review of paediatric patients with acute scrotum. ANZ J Surg 2003; 73:55–58.
    55. Atkinson GO Jr, Patrick LE, Ball TI Jr, Stephenson CA, Broecker BH, Woodard JR. The normal and abnormal scrotum in children: evaluation with color Doppler sonography. Am J Roentgenol 1992; 158:613–617.
    56. Kass EJ, Stone KT, Cacciarelli AA, Mitchell B. Do all children with an acute scrotum require exploration? J Urol 1993; 150 (Pt 2):667–669.
    57. Steinhardt GF, Boyarsky S, Mackey R. Testicular torsion: pitfalls of color Doppler sonography. J Urol 1993; 150 (Pt 1):461–462.
    58. Kaye JD, Shapiro EY, Levitt SB, Friedman SC, Gitlin J, Freyle J, Palmer LS. Parenchymal echo texture predicts testicular salvage after torsion: potential impact on the need for emergent exploration. J Urol 2008; 180 (Suppl):1733–1736.
    59. Lam WW, Yap TL, Jacobsen AS, Teo HJ. Colour Doppler ultrasonography replacing surgical exploration for acute scrotum: myth or reality? Pediatr Radiol 2005; 35:597–600.
    60. Kalfa N, Veyrac C, Lopez M, Lopez C, Maurel A, Kaselas C, et al.. Multicenter assessment of ultrasound of the spermatic cord in children with acute scrotum. J Urol 2007; 177:297–301. discussion 301.
    61. DaJusta DG, Granberg CF, Villanueva C, Baker LA. Contemporary review of testicular torsion: new concepts, emerging technologies and potential therapeutics. J Pediatr Urol 2013; 9 (Pt A):723–730.
    62. Burgu B, Aydogdu O, Huang R, Soygur T, Yaman O, Baker L. Pilot feasibility study of transscrotal near infrared spectroscopy in the evaluation of adult acute scrotum. J Urol 2013; 190:124–129.
    63. Nadel NS, Gitter MH, Hahn LC, Vernon AR. Preoperative diagnosis of testicular torsion. Urology 1973; 1:478–479.
    64. Nakielny RA, Thomas WE, Jackson P, Jones M, Davies ER. Radionuclide evaluation of acute scrotal disease. Clin Radiol 1984; 35:125–129.
    65. Yuan Z, Luo Q, Chen L, Zhu J, Zhu R. Clinical study of scrotum scintigraphy in 49 patients with acute scrotal pain: a comparison with ultrasonography. Ann Nucl Med 2001; 15:225–229.
    66. Paltiel HJ, Connolly LP, Atala A, Paltiel AD, Zurakowski D, Treves ST. Acute scrotal symptoms in boys with an indeterminate clinical presentation: comparison of color Doppler sonography and scintigraphy. Radiology 1998; 207:223–231.
    67. Terai A, Yoshimura K, Ichioka K, Ueda N, Utsunomiya N, Kohei N, et al.. Dynamic contrast-enhanced subtraction magnetic resonance imaging in diagnostics of testicular torsion. Urology 2006; 67:1278–1282.
    68. Yilmaz E, Hizli F, Afşarlar ÇE, Demirtaş C, Apaydin S, Karaman İ, Karaman A. Early diagnosis of testicular torsion in rats by measuring plasma D-dimer levels: comparative study with epididymitis. J Pediatr Surg 2015; 50:651–654.
    69. Sidler D, Brown RA, Millar AJ, Rode H, Cywes S. A 25-year review of the acute scrotum in children. S Afr Med J 1997; 87:1696–1698.
    70. Loh HS, Jalan OM. Testicular torsion in Henoch–Schonlein syndrome. Br Med J 1974; 2:96–97.
    71. Kaplan GW. Acute idiopathic scrotal edema. J Pediatr Surg 1977; 12:647–649.
    72. Urwin GH, Kehoe N, Dundas S, Fox M. Testicular infarction in a patient with sickle cell trait. Br J Urol 1986; 58:340–341.
    73. Jordan GH. Segmental hemorrhagic infarct of testicle. Urology 1987; 29:60–63.
    74. Baer HM, Gerber WL, Kendall AR, Locke JL, Putong PB. Segmental infarct of the testis due to hypersensitivity angiitis. J Urol 1989; 142:125–127.
    75. Eshel G, Vinograd I, Barr J, Zemer D. Acute scrotal pain complicating familial Mediterranean fever in children. Br J Surg 1994; 81:894–896.
    76. Baratelli GM, Vischi S, Mandelli PG, Gambetta GL, Visetti F, Sala EA. Segmental hemorrhagic infarction of testicle. J Urol 1996; 156:1442.
    77. Burgher SW. Acute scrotal pain. Emerg Med Clin North Am 1998; 16:781–809.
    78. Gofrit ON, Rund D, Shapiro A, Pappo O, Landau EH, Pode D. Segmental testicular infarction due to sickle cell disease. J Urol 1998; 160 (Pt 1):835–836.
    79. Moharib NH, Krahn HP. Acute scrotum in children with emphasis on torsion of spermatic cord. J Urol 1970; 104:601–603.
    80. Méndez R, Tellado M, Montero M, Ríos J, Vela D, Pais E, et al.. Acute scrotum: an exceptional presentation of acute nonperforated appendicitis in childhood. J Pediatr Surg 1998; 33:1435–1436.
    81. Manson AL. Mumps orchitis. Urology 1990; 36:355–358.
    82. Anderson MJ, Dunn JK, Lipshultz LI, Coburn M. Semen quality and endocrine parameters after acute testicular torsion. J Urol 1992; 147:1545–1550.
    83. Tryfonas G, Violaki A, Tsikopoulos G, Avtzoglou P, Zioutis J, Limas C, et al.. Late postoperative results in males treated for testicular torsion during childhood. J Pediatr Surg 1994; 29:553–556.
    84. Schalamon J, Ainoedhofer H, Schleef J, Singer G, Haxhija EQ, Höllwarth ME. Management of acute scrotum in children – the impact of Doppler ultrasound. J Pediatr Surg 2006; 41:1377–1380.
    85. Miller DC, Peron SE, Keck RW, Kropp KA. Effects of hypothermia on testicular ischemia. J Urol 1990; 143:1046–1048.
    86. Kass EJ, Lundak B. The acute scrotum. Pediatr Clin North Am 1997; 44:1251–1266.
    87. Thurston A, Whitaker R. Torsion of testis after previous testicular surgery. Br J Surg 1983; 70:217.
    88. Rodriguez LE, Kaplan GW. An experimental study of methods to produce intrascrotal testicular fixation. J Urol 1988; 139:565–567.
    89. Kutikov A, Casale P, White MA, Meyer WA, Chang A, Gosalbez R, Canning DA. Testicular compartment syndrome: a new approach to conceptualizing and managing testicular torsion. Urology 2008; 72:786–789.
    90. Belker AM. Re: Kutikov et al.: testicular compartment syndrome: a new approach to conceptualizing and managing testicular torsion (Urology 2008;72:786–789). Urology 2009; 73:684. author reply 685.
    91. Figueroa V, Pippi Salle JL, Braga LH, Romao R, Koyle MA, Bägli DJ, Lorenzo AJ. Comparative analysis of detorsion alone versus detorsion and tunica albuginea decompression (fasciotomy) with tunica vaginalis flap coverage in the surgical management of prolonged testicular ischemia. J Urol 2012; 188:1417–1422.
    92. Cornel EB, Karthaus HF. Manual derotation of the twisted spermatic cord. BJU Int 1999; 83:672–674.
    93. Ayan M, Tas U, Sogut E, Cayli S, Kaya H, Esen M, et al.. Protective effect of thymoquinone against testicular torsion induced oxidative injury. Andrologia 2016; 48:143–151.
    94. Beheshtian A, Salmasi AH, Payabvash S, Kiumehr S, Ghazinezami B, Rahimpour S, et al.. Protective effects of sildenafil administration on testicular torsion/detorsion damage in rats. World J Urol 2008; 26:197–202.
    95. Erol B, Tokgoz H, Hanci V, Bektas S, Akduman B, Yencilek F, et al.. Vardenafil reduces testicular damage following ischemia/reperfusion injury in rats. Kaohsiung J Med Sci 2009; 25:374–380.
    96. Wu ZG, Wang GB, Xiao YB, Chen TK, Cai J, Li CD. Protective effect of tadalafil against ischemia–reperfusion injury in rats. Zhonghua Nan Ke Xue 2015; 21:214–218.
    97. Karakaya E, Ateş O, Akgür FM, Olguner M. Rosuvastatin protects tissue perfusion in the experimental testicular torsion model. Int Urol Nephrol 2010; 42:357–360.
    98. Şener TE, Yüksel M, Özyilmaz-Yay N, Ercan F, Akbal C, Şimşek F, Şener G. Apocynin attenuates testicular ischemia–reperfusion injury in rats. J Pediatr Surg 2015; 50:1382–1387.
    99. Bozlu M, Coşkun B, Cayan S, Acar D, Aktaş S, Ulusoy E, Akbay E. Inhibition of poly(adenosine diphosphate-ribose) polymerase decreases long-term histologic damage in testicular ischemia–reperfusion injury. Urology 2004; 63:791–795.
    100. Erol B, Bozlu M, Hanci V, Tokgoz H, Bektas S, Mungan G. Coenzyme Q10 treatment reduces lipid peroxidation, inducible and endothelial nitric oxide synthases, and germ cell-specific apoptosis in a rat model of testicular ischemia/reperfusion injury. Fertil Steril 2010; 93:280–282.
    101. Hekimoglu A, Kurcer Z, Aral F, Baba F, Sahna E, Atessahin A. Lycopene, an antioxidant carotenoid, attenuates testicular injury caused by ischemia/reperfusion in rats. Tohoku J Exp Med 2009; 218:141–147.
    102. Akgul T, Karaguzel E, Surer H, Yağmurdur H, Ayyildiz A, Ustün H, Germiyanoğlu C. Ginkgo biloba (EGB 761) affects apoptosis and nitric-oxide synthases in testicular torsion: an experimental study. Int Urol Nephrol 2009; 41:531–536.
    103. Kanter M. Protective effects of melatonin on testicular torsion/detorsion-induced ischemia–reperfusion injury in rats. Exp Mol Pathol 2010; 89:314–320.
    104. Payabvash S, Salmasi AH, Kiumehr S, Tavangar SM, Nourbakhsh B, Faghihi SH, Dehpour AR. Salutary effects of N-acetylcysteine on apoptotic damage in a rat model of testicular torsion. Urol Int 2007; 79:248–254.
    105. Ergur BU, Kiray M, Pekcetin C, Bagriyanik HA, Erbil G. Protective effect of erythropoietin pretreatment in testicular ischemia–reperfusion injury in rats. J Pediatr Surg 2008; 43:722–728.
    106. Hsiao CH, Ji AT, Chang CC, Cheng CJ, Lee LM, Ho JH. Local injection of mesenchymal stem cells protects testicular torsion-induced germ cell injury. Stem Cell Res Ther 2015; 6:113.
    Keywords:

    acute scrotum; acute scrotal pain; testicular torsion

    © 2016 Human Andrology