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1
Department of Radiology, Dartmouth-Hitchcock Medical Center, One Medical
Center Dr., Lebanon, NH 03756.
2
Dartmouth Medical School, Hanover, NH 03755.
3
Present address: 17509 59th Ave., N.W., Edmonton, Alta., T6MIHI, Canada.
4
Department of Pathology, Dartmouth-Hitchcock Medical Center, Lebanon, NH
03756.
Received August 2, 1999;
accepted after revision January 4, 2000.
Presented at the annual meeting of the American Roentgen Ray Society, New
Orleans, May 1999.
Abstract
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SUBJECTS AND METHODS. Testicles were obtained at autopsy from a series of 25 male cadavers (age range, 16-80 years; mean, 62 years). Eight subjects had a history of cancer. Ex vivo sonography was performed and two board-certified radiologists graded the testis by consensus as normal, heterogeneous, or "other abnormality" (cyst, dilated rete, echogenic focus, or halo). Microscopic pathology was obtained in all abnormal (sonographic or gross pathologic) testes. The severity of tubular sclerosis (atrophy) was graded on a scale of 0-3+ by a uropathologist.
RESULTS. No testicular tumors were detected. Sonography revealed normal testes in 33 specimens, heterogeneous in seven specimens, and other in 10 specimens (one cyst, two dilated rete, three halos, and seven echogenic foci). Histology revealed that all seven cases of mottled or heterogeneous testis corresponded to extensive (grades 2 and 3) regions of tubular sclerosis (atrophy). A new sonographic finding of the "halo" was attributable to a thickened, adherent tunica albuginea.
CONCLUSION. The prevalence of heterogeneous testes in this elderly population was 14% and represented seminiferous tubule atrophy and sclerosis. The prevalence of clinically occult testicular cancer or metastases in this autopsy subject group was nil. Older patients with a mottled or heterogeneous testis, normal color Doppler flow, and no palpable abnormality probably do not need sonographic follow-up.
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Sonography was performed ex vivo in a plastic tub, and testes were graded as heterogeneous or normal by two fellowship-trained sonologists with consensus before histologic examination. "Heterogeneous testis" was defined as a subtle ill-defined or patchy area of altered echogenicity usually hypoechoic relative to the normal testicular parenchyma or other testis. Testes with other nonheterogeneous findings were categorized according to the other findings: testicular cysts, dilated rete testis, echogenic foci (without acoustic shadowing), thickened hypoechoic border around the testis (halo), and masses.
After scanning, the tunica vaginalis testis was removed, and the testis was bivalved and serially sectioned at approximately 5-mm sections through the long axis of the entire testis. The plane of sectioning was adjusted to intersect needles placed at sonography. Each slice was examined grossly with the aid of an illuminating microscope. All testes that had sonographic or gross pathologic lesions were processed for histologic examination after staining with H and E.
Abnormal testes were routinely examined for the following features: dilatation and cystic changes in the rete testis, parenchymal (tubular or interstitial) calcifications, tubular atrophy, tubular sclerosis, and thickening of the tunica albuginea testis. "Tubular sclerosis" was defined as fibrous thickening of the walls of the seminiferous tubules, and "atrophy" as a decrease in tubule diameter and partial to complete loss of spermatogenesis (generally coexisting). The uropathologist graded testicular tubular sclerosis and atrophy on a scale of 0-3+, with 0 = normal tubules, 1 = mild sclerosis and atrophy, 2 = moderate sclerosis and atrophy, and 3 = severe sclerosis and atrophy.
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On sonography, no testicular tumors were noted. The testis was graded on sonography as normal in 33 specimens (66%), heterogeneous in seven (14%), and other in 10 (20%). Of the heterogeneous testes, four had one or two poorly demarcated hypoechoic areas (Fig. 2A,2B) and three had a diffuse mottling. Other lesions seen were one testicular cyst, two cases of dilated rete testis, and seven testes with echogenic foci. None of the other sonographic findings group had significant heterogeneity. Three specimens had a sonographic halo that corresponded to a thickened tunica albuginea testis that was adherent to the epididymis.
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The corresponding histology in all seven specimens with sonographic heterogeneity revealed extensive regions of grade 2 (n = 3) or grade 3 (n = 4) tubular atrophy and sclerosis. In the sonographically normal testes, 31 specimens were histologically normal (n = 27) or mildly atrophic (n = 4). Two testes were false-negative on sonography; in other words, they had normal findings on sonography with grade 2 (n = 1) or grade 3 (n = 1) atrophy (Fig. 3A,3B). Considering normal or grade 1 atrophy as negative pathology and grade 2 or 3 atrophy as positive pathology, ex vivo sonography of tubular atrophy and sclerosis had a sensitivity of 78%, specificity of 100%, positive predictive value of 100%, negative predictive value of 94%, and accuracy of 95%.
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One subject (18 years old), who died from sepsis and leukemia, had diffuse intravascular coagulation in both testes and other organs. One of the testes was graded heterogeneous (true-positive, Fig. 2A,2B), and the other was graded sonographically normal (false-negative). Both testes had moderate to severe tubular atrophy and sclerosis. The two testes with false-negative findings on sonography (one testis from an 18-year-old man and one from a 61-year-old man [Fig. 3A,3B]) were found to be almost completely replaced by severe atrophy and sclerosis.
Among the other sonographic findings, histologic analysis confirmed the presence of the intratesticular cyst (dilated rete cyst), and the dilated rete testis in two testes. It also confirmed the presence of thickened adherent tunica albuginea testis in the three testes with a sonographic halo (Fig. 4A,4B,4C). Of the seven echogenic foci noted on sonography, only two had corresponding positive histologic findings: one represented focal calcification (oxalate crystals) in the tubules and interstitium and one represented dense calcification in a vein. Five testes with echogenic foci had no abnormalities detected at pathology.
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This sonographic appearance places the radiologist in a quandary regarding suggestions for patient care. There are five options with regard to testicular sonographic findings: ignore the finding, continue serial sonographic surveillance, obtain another imaging study (usually MR imaging), biopsy, or surgery. We are uncomfortable with the first option because heterogeneous testes represent a reproducible sonographic abnormality. The last two options involve expensive or invasive procedures. As a result, we have suggested follow-up sonograms in these patients at 6-12 month intervals, lacking objective data to support this surveillance but adopting the approach some authors favor for testicular microlithiasis without a mass [2, 3]. The presence of tumor was considered unlikely given the lack of palpable abnormality and that the patients were beyond the age range (15-35 years) for most testicular cancers. Furthermore, most patients are not willing to face surgery or biopsy for an unclear indication or a finding of indeterminate significance.
Our study shows that all cases of heterogeneous testes in this largely elderly population corresponded to seminiferous tubule atrophy and sclerosis. One pair of testes (of an 18 year old) also had disseminated intravascular coagulation, which probably accounted for the heterogeneity along with the atrophy and sclerosis. The ex vivo sonograms had a high specificity and positive predictive value (100%) and a fairly high sensitivity (78%) for the detection of tubular atrophy and sclerosis. The heterogeneous testes did not correspond to primary or secondary testicular tumors, infarction, infection, or other abnormality, although these would be in the differential diagnosis. Disseminated intravascular coagulation accounted for the other findings at pathology that may have contributed to the heterogeneity seen on sonography.
Testicular tumor is the most worrisome possibility when one discovers an intratesticular lesion or mass. Primary testicular cancer is generally a disease of younger patients (<40 years) [4], but older patients may present with lymphoma, leukemia, or metastases. In patients older than 60 years, 50% of testicular tumors are lymphomas [5]. Of our 25 patients, eight had a history of cancer of various types and two of these were leukemia, which is the second most common metastasis to the testis after lymphoma. Lymphoma was not present in our small series of patients. No cases of primary or secondary malignancy were identified on sonography or at pathology. A testicular mass from a metastasis as the primary clinical presentation of disease is extremely rare. Prostate carcinoma is the most common primary site to involve the testis with metastasis [6].
Other intratesticular lesions in the differential diagnosis include orchitis (acute or chronic), infarction, and vasculitis. Orchitis may be patchy or involve the entire testis and usually presents as a hypoechoic mass. There are generally systemic signs or symptoms of an infection. Orchitis often presents with hypervascular flow on color Doppler imaging, an area we could not evaluate. Testicular infarction most often occurs in young patients with torsion, and generally the clinical symptons are the acute onset of scrotal pain and swelling and should not be mistaken for the symptoms of a heterogeneous testis. The gray-scale appearance may be similar, but infarction is usually diffusely hypoechoic (compared with normal contralateral testis) rather than focal or ill-defined areas of heterogeneity [7]. Color Doppler imaging may show absent or extremely hypovascular blood flow, as opposed to the normal blood flow we see with heterogeneous testes.
Disseminated intravascular coagulation is another disease process that may mimic a heterogeneous testis, and our subject with multiorgan disseminated intravascular coagulation had marked testicular disseminated intravascular coagulation as well as tubular atrophy and sclerosis.
One testis of this subject was sonographically graded heterogeneous (Fig. 2A,2B) and the other one normal, an example of a false-negative finding on sonography, probably because virtually the entire testes was replaced by atrophy, sclerosis, and disseminated intravascular coagulation. This subject's grade 3 testicular atrophy and sclerosis was presumably caused by the chemotherapy and the severity of disease (acute lymphocytic leukemia). Sonography did not help differentiate the two coexistent causes. Vasculitis involves vessels in a manner similar to disseminated intravascular coagulation and may also present as a heterogeneous testis; therefore, in the proper clinical setting vasculities should be considered as a cause of heterogeneity in testes.
The underlying histologic changes may explain the hypoechoic geographic appearance of the heterogeneous testis. As the testis ages normally, cellular elements (spermatogonia) in the seminiferous tubules are lost, usually in conjunction with thickening of the tubular wall [8] (Fig. 5), probably caused by ischemia. Concomitant with this change is an increased peritubular acellular fibrosis of the interstitium. The peritubular sclerosis and tubular hyalinization are probably caused by the sparse and poorly organized capillary bed in the testis of elderly men [9]. These developments account for the more hypoechoic echotexture of the testis; there are fewer germ cells to provide acoustic interfaces and, as a result, the testis shows decreased echogenicity. Therefore, it seems reasonable that testicular atrophy and sclerosis is accompanied by subtle ill-defined (usually hypoechoic) alterations in echogenicity.
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In older men in the general population, heterogeneous testes are not enlarged and may even be smaller than normal (another sign of atrophy), show normal color or power Doppler flow, and have no palpable abnormalities. Heterogeneous testes are generally bilateral, although sometimes markedly asymmetric. The few cases we have followed with serial sonograms show static or slightly increased heterogeneity, presumably from increasing atrophy or sclerosis.
Of course, one must always be circumspect in extrapolating the results of an autopsy study to patients. The decision to evaluate this sonographic finding in an autopsy group was based on the relative ease of pathologic correlation. Ideally, a study would be designed with biopsy confirmation, but patients are understandably reluctant to undergo biopsy.
Testes were scanned in a small pilot study both without and with fixation, and fresh cadaveric testes were soon discarded as being unworkable. Specimens started to decompose almost immediately after removal from the body and localizing a lesion with a needle was difficult. The presence of fixation did not appear to add any sonographic artifacts, based on our pilot data. We also scanned fixed specimens with direct contact and water-bath scanning and chose the former because it is simpler for marking lesions with a needle and equal in resolution to water-bath scanning. With direct-contact scanning of the fixed specimens, we are able to reproduce the areas of heterogeneity we encounter among patients in our sonography laboratory.
The presence of a testicular "halo" was unexpected and one we have not found reported in the radiology or sonography literature. This hypoechoic rim represented the thickened tunica albuginea testis that was adherent to the epididymis. No significant scrotal history (trauma or infection) was documented in the medical charts of these two subjects, but the halo may have represented the sequela of prior trauma, infection, or inflammation. We have subsequently encountered this finding in one patient seen in our department. The significance of this finding warrants further investigation.
Einstein et al. [1] found eight cases of pathologically proven tubular sclerosis and interstitial fibrosis in 434 scrotal sonographic examinations. Only two of the eight cases had a palpable abnormality, and these two abnormalities were described as "spongy and subtle" in one patient and "cystic" in the other. However, in comparison with our more typical, ill-defined heterogeneous testes, their cases had sonographic findings that were reported to be indistinguishable from those of testicular malignancies, and hence underwent surgical evaluation. They also described both hypoechoic and hyperechoic lesions caused by the fibrosis; we encountered no examples of hyperechoic areas representing tubular atrophy or sclerosis. That study encompassed sonographic examinations of 8-10 years ago, and it is likely that the differences in results may reflect technologic advances with higher resolution sonography equipment.
Several limitations are recognized in our study. There were only seven cases of heterogeneous testes found on sonography. We did not analyze every testis histologically, only those that had sonographic or gross pathologic findings. As a result, we may have missed small areas of atrophy or sclerosis, vasculitis, or infarction. The true sonographic appearance may have been altered by decomposition in the postmortem state or by formalin-related artifacts, but all testes were placed in formalin within 1-2 hr after removal from the body and our pilot study did not have any of these problems. We also did not examine any testes with newer high-resolution equipment (e.g., 5000, Advanced Technology Laboratories; or Elegra, Siemens, Issaquah, WA), which we did not have at the time of the study. These higher resolution machines may have even increased the prevalence of heterogeneous testis seen in our series.
In conclusion, the prevalence of a heterogeneous testis in our series of primarily older men was 14%. The presence of a heterogeneous testis in an older patient (>50 years old) in the absence of a testicular mass suggests tubular atrophy and sclerosis. These testes probably do not have to be sonographically followed up unless there is a strong risk factor, such as a previous testicular cancer or a known extratesticular malignancy (prostate, lung), which can metastasize to the testes. In these cases, an annual sonogram is probably sufficient given the low likelihood of tumor. In the setting of a palpable testicular abnormality, regardless of the sonographic findings, testicular cancer must be excluded and the patient referred for urologic evaluation.
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