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Original Research |
1 Department of Radiology, Children's National Medical Center, 111 Michigan
Ave., NW, Washington, DC 20010.
2 Department of Urology, Children's National Medical Center, Washington, DC
20010.
Received April 14, 2005;
accepted after revision November 10, 2005.
Address correspondence to A. R. Nussbaum Blask
(ablask{at}cnmc.org).
Abstract
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MATERIALS AND METHODS. The sonograms of 50 pediatric patients (age range, neonate-17 years) with testicular torsion were retrospectively reviewed for the size, appearance, and blood flow of the epididymis. Medical records were reviewed for surgical and pathologic findings and to determine whether testicular salvage had been possible.
RESULTS. The epididymis was enlarged (maximum dimension, 5.5 cm) in 47 of the 50 patients with acute or late phase torsion and after manual or spontaneous detorsion. The average difference in volume between the ipsilateral epididymis and the contralateral epididymis was 30 cm3, highly significant (p < 0.0001). The shape of the epididymis was altered in 92% of the cases (globular, bilobular, or multilobular). Seventy-three percent showed increased echogenicity and 27% appeared isoechoic. Of those with active torsion, 93% of the epididymides were avascular; 2%, hypovascular; and 5%, hypervascular. After detorsion, 100% of the epididymides (10/10) had blood flow. In patients with testicular loss due to infarction, pathology showed engorgement and enlargement of the epididymis with hemorrhagic infarction. In one patient with a hypervascular epididymis, surgery showed inflammation and erythema of the epididymis. Testicular loss occurred in each type of epididymal flow pattern.
CONCLUSION. A markedly enlarged, echogenic, and avascular or hypovascular epididymis is an ancillary sonographic sign in pediatric patients with testicular torsion. A hypervascular enlarged epididymis infrequently occurs (5% of cases) and should not be mistaken for epididymitis. In addition, the return of epididymal blood flow is an ancillary sign of successful testicular detorsion.
Keywords: color Doppler sonography • emergency radiology • epididymis • genitourinary tract imaging • pediatric radiology • testicular torsion
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Radiologic imaging studies are performed frequently in the acutely symptomatic patient to avoid unnecessary surgical exploration. Over the past several years, testicular color Doppler sonography has become the initial imaging study of choice because of its reported high sensitivity (78.6-89%) and specificity (77-100%), coupled with its lack of radiation and rapidity of performance, replacing testicular scintigraphy in most cases [3-6]. In our institution, scintigraphy recently has served as an ancillary second study reserved for cases that were indeterminate for torsion on sonography or showed decreased—but still present—flow compared with the asymptomatic side.
The role of power Doppler sonography in the examination of the testes has been investigated. Whether it provides an additional advantage over color Doppler sonography or might, in fact, increase the false-negative rate because of its increased sensitivity to decreased but still present arterial blood flow is not yet known [7-11]. In several reports, researchers have described false-negative color Doppler sonography findings in patients with testicular torsion despite its high reported sensitivities [12-15]. In addition, seeing flow in the normal prepubertal testis may be difficult or impossible, making the diagnosis of torsion on the contralateral symptomatic side more difficult [3, 4, 10, 11, 16]. In fact, some authors have suggested that radionuclide scintigraphy remain the imaging technique of choice in prepubertal children [10].
In our previous study of 46 pediatric patients with an acute scrotum, we observed that a markedly enlarged avascular epididymis was present in children with torsion of the testis; it was a source of confusion in several cases because of its masslike appearance [3]. In this study, we retrospectively reviewed a series of pediatric patients with the known diagnosis of testicular torsion, including 13 patients with torsion from our previous study, to determine the frequency of this finding on testicular sonography. Also, we wanted to determine whether an abnormal appearance of the epididymis might be a useful ancillary gray-scale and color Doppler sign of testicular torsion. In addition, we wanted to see whether there were any differences in the appearance of the epididymis during acute phase torsion, during late phase torsion, or after spontaneous or manual detorsion, and we wanted to correlate the appearance of the epididymis with pathologic and surgical findings. Our final aim was to determine whether the sonographic appearance of the epididymis could be of any assistance in predicting testicular salvage.
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The size of the epididymis on both the symptomatic and the contralateral asymptomatic sides was determined. Sonographic studies had been performed using a standardized method to obtain longitudinal images parallel to the long axis of the testis and transverse images perpendicular to the long axis of the testis. The length and depth of the entire visualized portion of the epididymis were measured with calipers on a single longitudinal image in the plane of maximal enlargement. The transverse measurement was obtained from a single transverse image in the plane of maximal enlargement.
On the symptomatic side, if only the head was enlarged and the head was the only portion of the epididymis visualized, it was used for the measurements of epididymal size. A range of sizes was obtained for the symptomatic side and for the asymptomatic side. The epididymal size in the asymptomatic hemiscrotum served as the control sample in 41 of the 50 patients because there were no cases of bilateral synchronous testicular torsion. In the remaining nine patients, the epididymis in the asymptomatic hemiscrotum could not be measured retrospectively because images were insufficient or the epididymis was not seen or because of prior removal or atrophy of the contralateral testis and epididymis (two patients). In eight of these nine patients, the epididymis in the symptomatic hemiscrotum was matched to that of an age-matched control subject. In one of the nine patients, no quantitative analysis was performed because of the lack of hard-copy images. Evaluation was qualitative only and based on the written report.
The shape of each epididymis in the symptomatic hemiscrotum was categorized as triangular, round, or ovoid, and an estimated volume was obtained using the formula for a pyramid, sphere, or prolate ellipsoid, respectively, in 49 of the 50 patients. The estimated volume of the normal epididymis was calculated using the formula for a pyramid because review of the images in our series indicated the shape of the normal epididymis was best approximated by the triangular shape; none was globular, bilobular, or multilobular.
Other authors have previously described the shape of the normal epididymis as pyramidal [17, 18]. Leung et al. [18] in their sonographic analysis of 40 asymptomatic men suggested that the epididymis has a triangle, crescent, or teardrop shape. The volume of the epididymis on the symptomatic side was compared with that of the contralateral normal epididymis using a Student's t test of the difference between the means. Before statistical tests were applied, the data were checked for normality and homogeneity of variance. Normalizing variance-stabilizing data transformations were applied to satisfy the criteria for parametric analysis before testing. Thereafter, a Student's t test was applied to test whether the difference in epididymal volume between the symptomatic side and the asymptomatic side was a value other than zero. The portion of the epididymis that was enlarged was documented as the head, head and body, body and tail, head and tail, or entire epididymis.
The gray-scale appearance of the epididymis was evaluated. The shape was further analyzed to determine if it maintained a triangular configuration or if it was distorted into a globular, bilobular, or multilobular shape. The echotexture of the epididymis on the side of testicular torsion was evaluated and characterized as isoechoic or hyperechoic and as homogeneous or heterogeneous in texture. The number of epididymides containing multiple prominent cystic spaces was tabulated.
The vascularity of the ipsilateral epididymis and the symptomatic testis was evaluated in all 50 subjects with color flow Doppler imaging using low-flow settings (HDL 3000 or 5000, ATL). Each sonographic examination was performed by one of three experienced pediatric sonographers. The epididymis was characterized as vascular if color flow was seen, avascular if no color flow was detected, and hypovascular if only minimal flow was seen. If the epididymal flow was greater than the flow seen in the asymptomatic side, it was considered hypervascular. Pulsed Doppler tracings of the epididymis were not obtained except in two patients. The Doppler findings in the symptomatic testis were correlated with the findings in the ipsilateral epididymis. The number of cases with manual detorsion or spontaneous detorsion was tabulated, and color Doppler examinations were assessed both before and after detorsion, if available, or only after detorsion if sonography had not been performed before detorsion.
The patients' medical records were reviewed for surgical and pathologic findings and to determine whether testicular salvage had been possible.
The diagnosis of testicular torsion was established by surgery in 48 of the 50 patients; by late testicular atrophy in one patient; and by nuclear scintigraphy performed 24 hours after the initial sonography in one patient, whose parents declined giving consent for surgical intervention. Scans were divided into those showing acute phase versus late phase torsion on the basis of the duration of each patient's symptoms, as described by Chen et al. [19]: Acute phase torsion was defined as < 24 hours of pain and late phase torsion as 3 24 hours of pain.
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The epididymal size on the symptomatic side ranged from
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The shape of the epididymis was altered in acute phase or late phase torsion and after manual or spontaneous detorsion. The epididymis maintained a triangular configuration in the remaining 8% of cases. In the cases in which the normal triangular configuration was lost, the shape was globular (87%), bilobular (9%), or multilobular (4%) (Figs. 1A, 1B, 1C).
The echotexture of the epididymis was altered in patients with acute phase or late phase torsion and in those examined after manual or spontaneous detorsion. The most common pattern was markedly increased echogenicity (36/49 [73%]), either heterogeneous with increased foci (n = 29 cases) or homogeneous with a diffuse increase in echogenicity (n = 7) (Figs. 1A, 1B, 1C). Less commonly, the epididymis was isoechoic (13/49 [27%]).
Multiple cystic spaces were seen in 13 cases. Six of these cases showed no flow in the epididymis or cystic spaces because they were evaluated after testicular detorsion only. Two of the cases with cystic spaces were in the patients with testicular torsion and hyperemic epididymides, and most of the areas of sonolucency were confirmed to be vascular channels on the available color Doppler images. Because of the retrospective nature of our study, we could not determine if the other spaces without color fill-in were vascular channels as well or if they were areas of necrosis, hemorrhage, or thrombus within vessels. In the five other cases examined after manual or spontaneous detorsion, most, but again not all, of the cystic and tubular spaces were confirmed to be vascular. In two of the latter patients examined both before and after detorsion, the cystic spaces were seen to be primarily vascular channels that filled in with color on Doppler imaging after detorsion (Figs. 2A, 2B, 2C).
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Of the 43 patients with active torsion at the time of sonography, the epididymis was avascular in 40 patients, hypovascular in one patient, and hypervascular in two patients (Figs. 3A, 3B, 3C). Of the 10 patients who were examined after detorsion, either manual or spontaneous, all epididymides were vascular and six of the 10 were hypervascular. Of the three cases examined before and after detorsion, the transition from no epididymal flow to epididymal flow was observed, similar to the observation of flow in the corresponding testis (Fig. 2A, 2B, 2C, 2D). The testis was also avascular in 34 of the 40 patients, whereas it was hypovascular in the remaining six patients with an associated avascular epididymis. The testis also showed decreased flow in the one patient with a hypovascular epididymis and acute phase torsion. In the two patients with unexpected epididymal hyperemia, the testis was avascular in one and hypovascular in the second. In the former, scintigraphy also showed increased flow to the epididymis and a photon-deficient testis.
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Surgery and pathologic examination of 30 patients with testicular loss and avascular epididymis, as shown by the Doppler flow pattern, showed engorgement and enlargement of the epididymis with hemorrhagic infarction (Fig. 4). Two surgical cases after detorsion showed congestion of the distal spermatic cord. No other surgical or pathologic report included an evaluation of the size of the spermatic cord. Information about the degree of torsion of the spermatic cord was available in 11 cases. Seven patients with late phase torsion had from 540° to 720° or more of cord torsion with both an avascular epididymis and avascular testis at sonography; testicular salvage was not possible. In one patient with acute phase torsion with a twist of 540-720° who had both avascular epididymis and avascular testis, testicular salvage was successful. In three patients, a 360° twist of the spermatic cord was seen. One of the three patients had late phase torsion and an avascular epididymis and avascular testis; testicular salvage was not possible. The second case was also in a patient with late phase torsion with an avascular epididymis, minimal flow in the testis, and no testicular salvage. The third was a patient with acute phase torsion and a hyperemic epididymis, avascular testis, and testicular salvage.
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Surgery revealed an inflamed erythematous epididymis in one of the two patients with a hyperemic epididymis. The testis, which appeared avascular at Doppler imaging, was ischemic with 360° of torsion but was salvaged; the patient had a 12-hour history of pain (Fig. 3C). In the second case of hyperemic epididymis, surgery revealed hemorrhagic infarction of the epididymis, and testis salvage was not possible; that patient had a 20-hour history of pain and minimal flow in the testis at Doppler imaging (Figs. 3A and 3B).
The success rates of immediate testicular salvage were assessed. Of the 17 patients with acute phase torsion, two experienced testicular loss: One had a delay in treatment and the other had testicular infarction with a history of 20 hours of pain. Of the remaining 15 patients with acute torsion, the testis was salvaged. In 14 of 15, pain was present for 7 hours or less, and in the remaining patient, pain was present for 12 hours. Three of the 33 testes in late phase torsion were not removed because of possible viability. These three testes subsequently atrophied, and testicular salvage was not possible in any of the remaining cases of late phase torsion. Testicular loss occurred in each type of epididymal flow pattern.
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Our sonographic study suggests that an analysis of the appearance and vascularity of the epididymis will add ancillary information that may assist in the diagnosis of testicular torsion in pediatric patients and that an awareness of the associated finding of epididymal enlargement may avoid confusion with a mass or erroneous diagnosis of epididymitis, even though the diagnosis of testicular torsion is still primarily based on the flow pattern in the testis. Enlargement of the spermatic cord may also be a finding associated with testicular torsion [20-24].
Our study population consisted of pediatric patients with a proven diagnosis of either acute or late phase testicular torsion over a 10-year period. This review showed that enlargement of the epididymis in conjunction with altered echotexture, most frequently increased echogenicity, was a consistent finding in almost all of the cases. This appearance was also present in the patients who were examined after spontaneous or manual detorsion of the testis. Although the retrospective nature of the study necessitated epididymal measurements from 2D images, rather than the more ideal 3D volumetric measurements, the same methodology was applied to evaluate both the symptomatic and the asymptomatic hemiscrotum and the differences between the sides were highly significant. Also, although the estimated measurements were necessary for statistical analysis, epididymal enlargement—in conjunction with altered shape and echotexture in the symptomatic hemiscrotum—was visually obvious without comparison of epididymal measurements and was marked in most of the cases.
In the absence of or before manipulation of the testis or spontaneous detorsion, the epididymis was avascular or hypovascular on color Doppler sonography in 95% of the cases of acute or late phase torsion. Surprisingly, the epididymis was hyperemic in 5% of the cases of acute or late phase torsion (12% of the cases of acute torsion). Our sonographic evaluations of patients examined both before and after detorsion indicated that return of blood flow to the epididymis can be observed in real time, similar to flow to the testis, and can be used as additional evidence of a successful manual detorsion. Epididymal hyperemia was the predominant finding after testicular detorsion. Spontaneous detorsion should be a strong consideration in a patient whose pain has abated suddenly or who reports episodes of intermittent pain because epididymitis can have the same sonographic appearance.
Marked enlargement of the epididymis when the studies were initially performed was a confusing finding in several of our cases, and the possibility of an extratesticular mass or hematoma was considered. Enlargement of the epididymis in patients with testicular torsion has not been previously emphasized. However, our observations confirmed findings described previously by a few investigators. In one study, epididymal enlargement with hemorrhage was identified on gray-scale sonography in seven adult patients with testicular torsion [25]. The sonographic findings in seven pediatric patients with testicular torsion suggested a misleading diagnosis of tumor or epididymitis that resulted in delay of surgery and in testicular loss [12-15]. Four of these cases evaluated on color Doppler imaging showed testicular blood flow that was thought to be normal on the symptomatic side. In a recent case of testicular torsion that we reviewed, not part of this series, sonography showed avascular epididymal enlargement that was thought to be a tumor because flow was present within the testis in the symptomatic hemiscrotum. Diagnosis was delayed; a repeat study 9 hours after the first at our institution showed no testicular flow, and testicular loss occurred.
Retrospective review of the cases in our study group suggests that the diagnosis would have been altered or made earlier in two cases of testicular torsion, both of which resulted in testicular loss. The two cases of hyperemic epididymides had potential for delay in diagnosis because epididymitis with testicular ischemia was the leading sonographic diagnosis, but testicular torsion was thought to be the most likely diagnosis after testicular scintigraphy. Although two additional patients were prospectively thought to have traumatic testicular contusion with epididymal hemorrhage, the outcome would not have been different because both underwent surgical exploration and had late phase testicular torsion.
As these cases point out, an enlarged avascular epididymis has the potential to change or expedite the diagnosis in cases of acute torsion in which testicular flow is still present but is decreased or is still visually normal, because these cases may be interpreted as a false-negative. These cases are likely ones in which there are fewer degrees of spermatic cord torsion (partial torsion) and the patient presents earlier in the time course or has a thicker spermatic cord [21]. This sign theoretically has the potential to be of value when no testicular flow can be seen in the asymptomatic testis, although this did not occur in our series. Sanelli et al. [20] reported a case of partial torsion (360°) of the spermatic cord with visually normal color flow in the testis. They noted a masslike lobular appearance of the spermatic cord with a coiled configuration of the vessels and an elevated resistive index in the affected testis. Other authors have suggested that analysis of Doppler waveform patterns may also be helpful in cases of incomplete or partial torsion [26].
A study by Baud et al. [22] of patients with testicular torsion showed features that paralleled our results. They also described an extratesticular mass present in cases of testicular torsion, but not detorsion. They indicated the mass was due to the engorged, twisted spermatic cord. Kalfa et al. [23] suggested examining the spermatic cord along its complete length to detect a twist. They found that in all cases of torsion, even those with ambiguous testicular flow findings, sonography depicted the twist as a "snail shell-shaped mass." Arce et al. [24] also described additional sonographic findings related to specific color Doppler assessment of the spermatic cord.
In our series, the surgical, pathologic, and sonographic findings suggested that the extratesticular mass was primarily due to an enlarged epididymis. The mass not only was supratesticular in location, but also was frequently paratesticular and infratesticular. Also, a separate epididymal structure was not seen, and epididymal enlargement was present at pathologic examination. However, a portion or portions of the tissue cephalad to the testis could possibly have been an engorged spermatic cord merged with the epididymal head, even though this possibility could not be confirmed by retrospective review of the pathologic or surgical reports or by reanalysis of the sonograms. All of the sonograms were of the scrotum only; the inguinal regions were not examined.
Other causes of supratesticular masses need to be considered. Torsion of the testicular appendages may be associated with a supratesticular mass. However, the complete constellation of findings are dissimilar to those associated with testicular torsion; instead, a distinct 4- to 16-mm extratesticular extraepididymal avascular mass is identified in most cases at the upper pole of the testis (the epididymis testis or the appendix testis) in conjunction with an enlarged epididymis and testis with increased flow [27].
Isolated torsion of the epididymis has also been reported, although it seems to be a rare occurrence. A 9-year-old boy with acute scrotal pain, associated with a long, tortuous epididymis and long mesorchium, had this diagnosis established at surgery [28]. Clinically, tender swelling at the inferior pole of the testis was present and the testis was not tender to palpation. A sonogram was not obtained. Two other patients with an acute scrotum and with "dissociation of the testis and epididymis" have been reported, one in a 6 month old and one in an 18 year old [29]. The epididymis was completely infarcted in the infant, requiring epididymectomy.
In most of our patients, the absence of color Doppler flow in the enlarged epididymis was the key feature differentiating testicular torsion from inflammatory epididymitis. However, the epididymis infrequently was hyperemic— even when testicular torsion was present. Spectral analysis was not performed in either of our two patients with hyperemic epididymis, so whether the increase in flow was arterial or venous flow is not known. Recently, Arce et al. [24] described increased flow in the spermatic cord distal to the site of rotation and attributed it to venous engorgement. That theory could also explain the hyperemic epididymis cases in our series. Those cases were a diagnostic dilemma, and the possibility of epididymitis with secondary ischemia of the testis from venous outflow compromise was entertained [30]. The fact that the confirmed diagnosis was testicular torsion in both of these patients suggests that surgical exploration is warranted when an avascular or hypovascular testis is seen in conjunction with what appears to be a hyperemic epididymis, distal spermatic cord, or both.
If a patient has undergone known manual detorsion of the testis, the presence of flow within an enlarged epididymis and in the testis suggests manipulation was successful, as shown by the resumption of blood flow. In the patient whose acute symptoms have resolved, spontaneous detorsion should be considered when an enlarged hyperemic epididymis and testicular flow are present.
An analysis of the vascular supply to the scrotum and its contents explains these sonographic findings. The spermatic cord contains the testicular, deferential (artery of the ductus deferens), and cremasteric arteries. The testicular artery supplies the testis and epididymis, and the artery of the ductus deferens and cremasteric arteries supply the epididymis, vas deferens, and peritesticular tissues [19, 30]. The testicular artery is a branch of the abdominal aorta, and the artery of the ductus deferens is a branch of the superior vesical artery [31]. The epididymis therefore has a dual blood supply via the testicular artery and via its anastomosis with the artery of the ductus deferens [31]. The venous drainage of the scrotal contents also passes through the spermatic cord. Because the vascular supply of the epididymis passes through the spermatic cord, the twisting of the spermatic cord, similar to twisting of the testis, will compromise its blood supply and venous drainage. This explains the presence of epididymal enlargement and engorgement seen on sonographic examination and the ischemic changes identified at pathologic examination.
Our patients with hypervascular epididymides and lower cord complex associated with testicular torsion are more difficult to explain unless the artery to the ductus deferens, which travels centrally in the cord, cannot be compressed to the same degree as the testicular artery. Theoretically, vessels that do not pass through the spermatic cord, such as the pudendal vessels, may provide blood flow, although no anastomoses have been described. The scrotal wall derives its blood supply from branches of the pudendal artery, which do not pass through the spermatic cord and therefore maintain its supply during testicular torsion [19, 32]. In late phase torsion, peritesticular inflammatory changes occur and account for the halo of peripheral hypervascularity seen at both sonography and scintigraphy [32]. Alternatively, venous engorgement, due to obstruction of the distal spermatic cord as proposed by Arce et al. [24], is a possibility for the hypervascular epididymis.
Testicular viability depends on both the degree and the duration of torsion. After 10 hours of symptoms, most testes cannot be saved [33]. Some testes that are saved at surgery atrophy over time [33]. This occurred in three of our patients. In our series, an enlarged avascular epididymis was present in cases of both acute and late phase torsion; therefore, it was not a helpful sign for predicting which testes could be salvaged. Because we had only two cases of hyperemic enlarged epididymides with testicular torsion, one with and one without testicular salvage, whether this sign could be of any predictive value for testicular salvage is not known. In all of our patients with manual or spontaneous detorsion and reestablishment of blood supply to the testis and epididymis, immediate testicular salvage was achieved, even in those cases in which testicular flow after detorsion was diminished in comparison with the asymptomatic side.
The enlarged hyperechoic epididymis is a consistent finding in pediatric testicular torsion that may assist in the diagnosis of torsion, especially in the prepubertal testis and in difficult cases in which arterial supply to the testis is still maintained but is decreased. Sonographic findings and the associated management suggestions are summarized in Tables 1 and 2. The primary diagnosis of testicular torsion is, nevertheless, still based on testicular flow pattern. The epididymis can resemble an extratesticular mass or hematoma. The avascular or hypovascular nature of the epididymis in most cases of testicular torsion (95%) allows these cases to be distinguished from epididymitis, which can have a similar gray-scale appearance. An enlarged hyperemic epididymis that is not due to epididymitis may be seen infrequently in cases of torsion (5%).
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The epididymis, in addition to the testis, should be sonographically examined for return of color Doppler vascularity after spontaneous or manual detorsion; the presence of epididymal flow in conjunction with flow in the testis is additional evidence of successful detorsion. After detorsion, either manual or spontaneous, the epididymis is frequently hypervascular. The appearance of the epididymis is abnormal in both acute and late phase torsion, and its appearance does help not predict testicular salvage.
Acknowledgments
We thank Dr. Robert J. McCarter for performing the statistical analysis for
this project.
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