MRI in the Histologic Characterization of. testicular neoplasms.

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1 Tsili et al. MRI of Testicular Neoplasms Genitourinary Imaging Original Research 12_07_2267_Tsili.fm 11/9/07 thina C. Tsili 1 Constantine Tsampoulas 1 Xenofon Giannakopoulos 2 Dimitrios Stefanou 3 Yiannis lamanos 4 Nikolaos Sofikitis 2 Stavros C. Efremidis 1 Tsili C, Tsampoulas C, Giannakopoulos X, et al. Keywords: magnetic resonance, testicular tumors, testis DOI: /JR Received March 17, 2007; accepted after revision June 12, Department of Clinical Radiology, University Hospital of Ionnina, Leoforos S. Niarchou, 45500, Platia Pargis, 2, , Ioannina, Greece. ddress correspondence to. C. Tsili (a_tsili@yahoo.gr). 2 Department of Urology, University Hospital of Ionnina, Leoforos S. Niarchou, 45500, Ioannina, Greece. 3 Department of Pathology, University Hospital of Ionnina, Leoforos S. Niarchou, 45500, Ioannina, Greece. 4 Department of Hygiene and Public Health, Panepistimioupolis, Leoforos S. Niarchou, 45500, Ioannina, Greece. WE This is a Web exclusive article. JR 2007; 189:W331 W X/07/1896 W331 merican Roentgen Ray Society MRI in the Histologic Characterization of Testicular Neoplasms OJECTIVE. The purpose of our study was to investigate the potential role of MRI in the preoperative characterization of the histologic type of testicular tumors and, more specifically, to differentiate seminomatous from nonseminomatous testicular neoplasms. MTERILS ND METHODS. Twenty-one patients with histologically proven germ cell testicular tumors underwent MRI of the scrotum on a 1.5-T unit. T2- and T1-weighted sequences before and after IV administration of gadolinium chelate were performed. MRI studies were retrospectively reviewed by two radiologists and findings were correlated with the histopathologic diagnosis. n attempt was made to differentiate seminomatous from nonseminomatous testicular tumors on the basis of signal intensity and homogeneity of the lesions, presence of fibrovascular septa, tumor encapsulation, and patterns of contrast enhancement. Interobserver agreement was assessed using weighted kappa statistics. RESULTS. MRI findings correctly characterized 19 (91%) of 21 testicular neoplasms (nine seminomatous and 10 nonseminomatous testicular tumors), with excellent interobserver agreement. The presence of an intratesticular lesion of predominantly low signal intensity on T2-weighted images, with septa enhancing more than tumor tissue after contrast material administration, was more suggestive for the diagnosis of a seminoma. Tumors that were markedly heterogeneous both on unenhanced and contrast-enhanced images were indicative of a nonseminomatous neoplasm. CONCLUSION. Our study shows that MRI provides a credible preoperative differentiation of seminomatous from nonseminomatous testicular tumors, with excellent interobserver agreement. esticular cancer, although representing 1% of all malignancies in T men, is the most common neoplasm in boys and young adults from 15 to 34 years old [1]. The estimated number of new cases of testicular carcinoma in the United States during 2006 was 8,250, and cancer deaths due to this disease were estimated to occur in 370 patients [2]. Testicular cancer most commonly presents as a painless scrotal mass. Ninety-five percent of testicular carcinomas are germ cell tumors (GCTs) arising from the germinal epithelium of the seminiferous tubules. The GCT line is fairly evenly split between seminomas and nonseminomatous germ cell tumors (NSGCTs). Seminomas, which account for 35 50% of all GCTs [3, 4], are the most common type of testicular carcinoma and are encountered mostly during the fourth decade of life. NSGCTs typically occur earlier in life, usually during the third decade, and include embryonal carcinoma, teratoma, choriocarcinoma, and yolk sac tumor, although mixed tumors presenting with multiple histologic types are the most common (40%) [3, 4]. Sonography is currently the primary imaging technique in the assessment of scrotal disease [3, 5]. However, because of its wide field of view, multiplanar capabilities, and intrinsic high soft-tissue contrast, MRI may represent an efficient supplemental technique for scrotal imaging [6 11]. lthough the imaging features of testicular neoplasms reflect their gross morphology and histologic characteristics [4, 5, 12, 13], there are few reports in the English-language literature correlating the MRI findings of testicular neoplasms with their histologic characteristics [12, 14]. The purpose of this study was to investigate the potential role of MRI in the preoperative characterization of the histologic type of testicular tumors and, more specifically, to differentiate seminomatous from nonseminomatous testicular neoplasms. JR:189, December 2007 W331

2 Tsili et al. Materials and Methods We retrospectively reviewed the MRI examinations of 21 patients (age range, years; mean age, 30 years) with histologically proven testicular GCTs who were referred to the urology department because of a painless scrotal mass between March 2002 and January These patients constitute our study group. The institutional review board did not require approval or the patients informed consent for the review of medical records and MRI examinations. ll patients underwent sonography and MRI of the scrotum before orchiectomy. MRI Technique MRI was performed on a 1.5-T unit (Gyroscan or Intera, Philips Medical Systems) with the patient in the supine position. 17-cm circular surface coil was placed over the scrotum. xial spin-echo T1- weighted imaging (TR/TE, 650/15; slice thickness, 3 mm; gap, 0.5 mm; field of view, mm; and matrix, mm) was performed. This sequence with the addition of frequency-selective fat suppression was repeated whenever the supervising radiologist noted a lesion with high T1 signal intensity. No change of this high signal intensity on the fat-suppressed sequence was attributed to the presence of subacute hemorrhage, whereas a signal loss C Fig year-old man with left testicular seminoma. and, Coronal T2-weighted () and contrastenhanced T1-weighted () images show multinodular intratesticular mass lesion (arrows). Tumor is homogeneous and of low signal intensity on T2- weighted image () compared with normal testicular parenchyma. fter gadolinium administration, there is enhancement of tumor septa (). Imaging features suggest seminomatous lesion. Small right hydrocele (stars) is also seen. C, Photomicrograph of histologic section shows seminoma of classic type. Tumor cells are uniform with abundant clear cytoplasm and are arranged in nests outlined by fibrous bands. (H and E, 400) was considered diagnostic for the presence of fat. xial, coronal, and sagittal fast spin-echo T2- weighted images (4,000/100; slice thickness, 3 mm; gap, 0.5 mm; field of view, mm; and matrix, mm) were also obtained. Unenhanced axial turbo spin-echo T1-weighted images (525/15; slice thickness, 8 mm; gap, 0.8 mm; field of view, mm; matrix, mm) using the body coil covering the area from the aortic bifurcation to the renal hila were obtained to assess for the presence of retroperitoneal lymphadenopathy. Gadopentetate dimeglumine (Omniscan, GE Healthcare) was administered IV in all cases (0.2 mmol/kg) and spin-echo T1-weighted images covering the scrotal area in the axial, coronal, and sagittal planes using the same parameters as the unenhanced images were obtained. MR Image Interpretation MR image interpretation was performed by two radiologists with 4 and 2 years of experience in MRI of the scrotum. These radiologists did not have knowledge of the histopathologic findings. MR image interpretation included tumor detection and lesion characterization. Signal intensity of the lesions was compared with that of normal testicular parenchyma. The homogeneity or heterogeneity of the lesion signal was estimated, and the presence of tumor capsule was sought. reas of hyperintensity on T2-weighted images not enhancing after gadolinium administration were considered as areas of necrosis. The presence of hemorrhage or fat within the tumors was also recorded. andlike structures of low signal intensity on T2-weighted images enhancing after gadolinium administration were recognized as fibrovascular septa. Finally, patterns of contrast enhancement were recorded. On the basis of these findings, we made a step forward to differentiate seminomas from nonseminomatous testicular tumors. Seminomas, because of their cellular uniformity and nodular histologic characteristics (Fig. 1), were expected to exhibit signal homogeneity of low intensity on T2- weighted images. The presence of septa within the tumor was also considered to characterize seminomatous lesions. These septa were expected to enhance more than tumor tissue after gadolinium administration. NSGCTs were expected to have heterogeneous signal, with areas of hemorrhage or necrosis adding to their heterogeneity, especially after gadolinium administration, probably because of their extremely heterogeneous histologic appearance (Fig. 2). The coexistence of fat within these lesions was also considered compatible with the diagnosis of a nonseminomatous lesion (Fig. 3). The interobserver agreement on MR interpretation between the two radiologists was quantified by using weighted kappa statistics. Evaluation of MRI findings was retrospectively correlated with the histopathologic findings, which were the standard of reference. The histologic sections of each case were reviewed in retrospect by one pathologist with 25 years of experience in scrotal pathology, and the histologic findings were correlated with the MR diagnosis. Results Histologic examination of the surgical specimens disclosed the presence of 21 testicular neoplasms. Eleven were found to be nonseminomatous testicular tumors, including mixed NSGCTs: teratocarcinoma (n =4); embryonal carcinoma and seminoma (n =1); teratoma, embryonal carcinoma, and yolk sac tumor (n = 1); teratoma, embryonal carcinoma, choriocarcinoma, and yolk sac tumor (n = 1); embryonal carcinoma (n = 1); mature cystic teratoma (n = 2); and yolk sac tumor (n = 1). Ten neoplasms proved histologically to represent seminomas. MRI findings led to a correct histologic diagnosis in 19 (91%) of 21 cases. MRI enabled the correct preoperative characterization of nine of 10 seminomas. Three seminomas were recognized as multinodular, sharply defined, homogeneous tumors of low signal intensity W332 JR:189, December 2007

3 MRI of Testicular Neoplasms on T2-weighted images (Fig. 1). The other six cases were predominantly of low intensity on T2-weighted images but exhibited signal heterogeneity with small areas of hemorrhage (Fig. 4) in four cases and areas of necrosis in two cases. In all cases of seminomas, fibrovascular septa were detected within the tumors, showing greater enhancement than tumor tissue after gadolinium administration (Fig. 5). The number of septa was variable, ranging from less than five to numerous, the latter detected in cases of large neoplasms (Figs. 4 and 5). Septal thickness was also variable. In five seminomas, septa were thin, with thickness less than 3 mm, and in the other four cases, thick septa with thickness greater than 3 mm were found to coexist. Despite signal heterogeneity and presence of hemorrhage and necrosis in the six seminomatous lesions, these tumors were correctly characterized because of the presence of distinctive MRI features such as predominantly low signal intensity on T2-weighted images and the presence and enhancement of tumor septa. Ten testicular lesions were correctly characterized on MRI as nonseminomatous tumors. These lesions appeared as heterogeneous masses on T2-weighted images and C D Fig year-old man with teratocarcinoma of right testicle. and, Transverse () and sagittal () T2-weighted images depict left testicular mass (arrow, ; long arrow, ) with markedly heterogeneous signal. Tumor is surrounded by low-signal-intensity halo (long arrow, ), corresponding histologically to a fibrous capsule. There is invasion of the tunica albuginea by the tumor (short arrow, ). C, Sagittal contrast-enhanced T1-weighted image shows heterogeneous enhancement of tumor. reas of hyperintensity within lesion on T2-weighted images that did not enhance after gadolinium administration (arrows) proved histologically to represent areas of necrosis. Imaging features in this case suggest nonseminomatous lesion. D, Photomicrograph of histologic section shows heterogeneous tumor containing squamous epithelium, cartilage, and embryonic body (center of photo mixed teratoma and embryonal carcinoma). (H and E, 100) showed heterogeneous enhancement after gadolinium administration (Fig. 2). reas of necrosis were detected in six cases and areas of hemorrhage in seven. Included in the category of nonseminomatous tumors were two lesions detected with areas of high signal intensity and loss of signal on T1- and fat-suppressed T1-weighted images (Fig. 3), respectively, a finding diagnostic for the presence of fat. The presence of enhancement in the last two cases made it possible to diagnose these tumors as mature cystic teratomas proven histologically allowing us to differentiate them from an epidermoid cyst, which should always be considered in the presence of a fatcontaining mass within the testicles [15 17]. Nine of 10 nonseminomatous tumors and five of nine seminomas were surrounded by a lowsignal-intensity halo. This halo proved histologically to represent a fibrous capsule. MRI was incorrect in the preoperative diagnosis in one case of an embryonal carcinoma and another case of an anaplastic seminoma. In the first case, a testicular tumor was detected on T2-weighted images as relatively homogeneous and of low signal intensity. Therefore, it was characterized as a seminoma (Fig. 6), whereas in the second case, the lesion was markedly inhomogeneous on T2- weighted images, presenting large areas of necrosis and enhancing heterogeneously, therefore resembling closely a nonseminomatous lesion (Fig. 7). The MRI features in each individual case for the seminomas and the nonseminomatous testicular tumors are illustrated in Tables 1 and 2, respectively. The interobserver agreement between the readings of the two radiologists was excellent (κ =1.0). Discussion The distinction of GCTs in seminomatous and nonseminomatous neoplasms is important for determining treatment and prognosis. Seminomas have the best prognosis among GCTs because of their high sensitivity to radiation and chemotherapy. Nonseminomatous histologic features are associated with poor prognosis because they are not as radiosensitive as seminomas. Classic seminomas histologically are usually homogeneously solid, lobulated masses that may contain sharply circumscribed areas of necrosis. Microscopically, tumor cells are uniform with abundant clear cytoplasm characteristically arranged in nests outlined JR:189, December 2007 W333

4 Tsili et al. C D Fig year-old man with mature cystic teratoma of left testicle., Transverse T2-weighted image depicts sharply demarcated heterogeneous left intratesticular mass lesion (arrow). and C, Transverse T1-weighted () and fat-suppressed T1-weighted (C) images show areas (arrows) of high signal intensity and loss of signal on fat-suppressed images, compatible with presence of fat. D, Sagittal contrast-enhanced T1-weighted image shows lesion enhancement (arrow). C Fig year-old man with seminoma of left testicle. and, Coronal T2-weighted () and contrast-enhanced T1-weighted () images depict large left testicular mass. Tumor is heterogeneous but mainly of low signal intensity on T2-weighted image (). There are multiple septa (arrows, ) within the lesion, detected both on T2-weighted and contrast-enhanced T1-weighted images, suggesting diagnosis of seminoma. There is interruption of tunica albuginea by tumor (arrow, ), suggestive of invasion, which was proven histologically. Star indicates right testicle. C, Transverse T1-weighted image depicts small hyperintense focus (arrow) within mass, corresponding to area of hemorrhage. Star indicates right testicle. W334 JR:189, December 2007

5 MRI of Testicular Neoplasms C Fig year-old man with left testicle seminoma invading ipsilateral spermatic cord. C, Sagittal T2-weighted (), coronal T2-weighted (), and contrast-enhanced T1-weighted (C) images depict large tumor involving left testicle and invading epididymis and spermatic cord. Tumor is inhomogeneous but mainly hypointense on T2-weighted images. There are bandlike structures (arrows) within mass that are of low signal intensity on T2-weighted images. These structures enhance more than rest of tumor after gadolinium administration, indicating fibrovascular septa. D, Photomicrograph of histologic section shows testicular seminoma. Neoplastic cells infiltrate spermatic cord. (H and E, 100) by fibrous bands; in 80% of cases, these bands are infiltrated by lymphocytes and plasma cells, possibly due to a host reaction to the tumor. The imaging features of seminomas reflect their histologic characteristics and their uniform cellular nature. On MRI, seminomas usually appear as multinodular tumors of uniform signal intensity that are hypointense on T2-weighted images. andlike structures of low signal intensity on T2-weighted images may be detected within these tumors, corresponding to the fibrovascular septa. In our study, these septa showed greater enhancement than tumor tissue after gadolinium administration. These imaging features enabled a correct preoperative characterization for nine of 10 seminomas in this study, even in the cases where areas of necrosis or hemorrhage were found to coexist within the tumors. Imaging findings described for dysgerminoma, the ovarian counterpart of seminoma, are similar [13, 18 20]. These tumors are usually multilobulated, uniformly homogeneous, and have prominent septa, which enhance after IV contrast material administration [13, 18 20]. NSGCTs include a large group of histologically diverse neoplasms. Four basic types have been recognized: embryonal carcinoma, teratoma, choriocarcinoma, and yolk sac tumor. The combination of two or more types of these neoplasms results in mixed GCTs. D Fig year-old man with embryonal carcinoma of right testicle. Transverse T2-weighted image shows small tumor (arrow) involving right testicle. Lesion is relatively homogeneous and hypointense, suggesting diagnosis of seminoma. Some more common patterns are teratoma and embryonal carcinoma; seminoma and embryonal carcinoma; and teratoma, embryonal carcinoma, and yolk sac tumor. Embryonal carcinoma has grossly a more variable appearance than seminoma [3]. It is mainly a solid tumor containing foci of hemorrhage and necrosis. Microscopically, it is composed of undifferentiated cells or may show signs of early differentiation toward embryonic structures, trophoblast, or extraembryonic endoderm or mesoderm in the form of papillary or glandular formations. The tumor has a carcinomatous appearance; the cells are more anaplastic, with prominent variation in size and shape. Teratoma, on the other hand, macroscopically, is predominantly cystic and multiloculated [3]. Foci of cartilage are usually present within the tumor. ll types of tissues can be seen microscopically, most commonly nerve, cartilage, and various types of epithelium. These tumors are further divided into mature and immature teratomas and those with malignant areas. Dermoids, representing the most common teratomatous lesion in the ovary, constitute only a small minority of testicular teratomas [3, 4]. Choriocarcinomas represent the most lethal form of testicular carcinomas. These tumors are often small, usually hemorrhagic, and partially necrotic [3]. Yolk sac tumor has a soft consistency and a microcystic appearance [3]. Therefore, nonseminomatous testicular tumors are expected to appear as heterogeneous masses on MRI, with areas of hemorrhage or necrosis showing heterogeneous enhancement after gadolinium administration. JR:189, December 2007 W335

6 Tsili et al. Fig year-old man with anaplastic seminoma of right testicle. and, Coronal T2-weighted () and contrast-enhanced T1-weighted () images show large inhomogeneous right testicular mass invading ipsilateral epididymis (long arrow). Finding was confirmed on histology. ecause of mass heterogeneity, both on unenhanced and contrast-enhanced MR images, it was incorrectly characterized as nonseminomatous lesion. There is also small right hydrocele (short arrow, ). Star indicates left testicle. TLE 1: MRI Features for the 10 Seminomatous Tumors Patient MRI Features No. ge (y) Signal Homogeneity Low SI Necrosis Hemorrhage Capsule Septa Septal Enhancement Note Case 9 was incorrectly characterized as a nonseminomatous tumor. SI = signal intensity on T2-weighted images, + indicates present, indicates absent. TLE 2: MRI Features for the 11 Nonseminomatous Testicular Tumors Patient MRI Features No. ge (y) Signal Homogeneity Low SI Necrosis Hemorrhage Capsule Septa Heterogeneous Enhancement Note Case 5 was incorrectly characterized as a seminoma. SI = signal intensity on T2-weighted images, + indicates present, indicates absent. Our differential diagnosis was based on criteria, such as those described previously, and it was successful in 10 of 11 nonseminomatous testicular tumors. Tumor heterogeneity and heterogeneous enhancement proved the most valuable findings in the characterization of a nonseminomatous lesion. Schultz-Lampel et al. [14] succeeded in making a correct preoperative differentiation between seminomas and nonseminomatous tumors in 42 (62%) of 67 patients with testicular carcinomas in their study, although the exact criteria used for this differentiation are not described. Johnson et al. [12] in a study of 15 patients with GCTs showed that MRI could be used to provide a preoperative histologic classification of these tumors. y using T1- and T2-weighted sequences, the authors correctly characterized 13 (87%) of 15 neoplasms. The presence of a relatively homogeneous testicular mass of low signal intensity on T2-weighted images was considered indicative of a seminomatous lesion. On the other hand, a markedly heterogeneous mass with areas of necrosis or hemorrhage was characterized as a nonseminomatous lesion. It is suggested from our study that the presence of fibrovascular septa, seen on T1- or contrast-enhanced T2-weighted images, is indicative of a seminomatous lesion. Our MR protocol also included the administration of gadolinium chelate compounds and study of the patterns of enhancement of germ cell testicular neoplasms. In cases of seminomas, fibrovascular septa were found to enhance more than tumor tissue. On the other hand, nonseminomatous testicular tumors showed a markedly heterogeneous enhancement. reas that did not enhance were found histologically to represent areas of necrosis or hemorrhage. Using the above criteria, this study enabled the differentiation between seminomatous from nonseminomatous testicular tumors in 19 (91%) of 21 cases. The presence of a tumor capsule, seen on both seminomas and nonseminomatous tumors, could not be used in the preoperative differentiation of these tumors. Imaging has an important role in the investigation of scrotal masses, although physical examination represents the primary technique for the evaluation of scrotal abnormalities. Sonography is the standard imaging technique for the investigation of testicular lesions [5, 21 25]. It is easily performed, inexpensive, and has been shown to be 100% sensitive in the identification of scrotal masses. MRI of the scrotum has been used as an alternative technique for the diagnosis of scrotal disease W336 JR:189, December 2007

7 MRI of Testicular Neoplasms [6 11, 26 28]. It is a diagnostic tool of high performance for morphologic assessment and tissue characterization in the preoperative evaluation of scrotal masses. MRI can reduce the incidence of diagnostic surgical explorations for scrotal pathology. The technique has been proven highly accurate in the differentiation of extratesticular from intratesticular disease [10, 29 31], providing good results in the distinction between benign and malignant testicular masses [4, 32 34] and allowing the accurate evaluation of the local extent of the disease in cases of testicular carcinoma [10]. MRI is particularly recommended when sonographic findings are inconclusive or inconsistent with the clinical findings [34, 35]. Moreover, this study showed that MRI findings could be closely correlated with the histologic characteristics of testicular neoplasms, providing a preoperative classification of the histologic type of testicular tumors. potential criticism of our study is that although all patients underwent sonography and MRI of the scrotum, no direct comparison between the results of both techniques was performed. This was also a retrospective study of the MRI characteristics of a small number of testicular tumors (n = 21) in an attempt to preoperatively differentiate seminomatous from nonseminomatous testicular neoplasms, and perhaps there was some bias because most radiologists are familiar with the imaging features of these neoplasms [4, 5, 13]. The more important question is whether MRI offers the ability to differentiate testicular malignancies from benign intrascrotal lesions (such as focal testicular infarction, epidermoid cyst, or granulomatous orchitis), obviating an unwanted orchiectomy. This should be a point of a future research. Finally, a limitation of our MR protocol was that it did not include dynamic contrast-enhanced imaging to assess potential differences in enhancement patterns between seminomas and nonseminomatous testicular tumors. In conclusion, our study showed that MRI is able to provide a credible preoperative differentiation of seminomatous from nonseminomatous testicular tumors, with excellent interobserver agreement. The presence of an intratesticular lesion of predominantly low signal intensity on T2-weighted images with septa enhancing more than tumor tissue after contrast material administration is more suggestive for the diagnosis of a seminomatous lesion. Tumors that are heterogeneous both on unenhanced and contrast-enhanced images are indicative of a nonseminomatous neoplasm. References 1. Ulbright TM, min M, Young RH. Tumors of the testis, adnexa, spermatic cord and scrotum. In: Rosai J, Sobin LH, eds. tlas of tumor pathology, fasc 25, ser 3. 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