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Shear Wave Elastography Evaluation of Testes
in Patients With Varicocele
Hasan Erdogan, MD,* Mehmet Sedat Durmaz, MD,* Serdar Arslan, MD,* Funda Gokgoz Durmaz, MD,
†
Hakan Cebeci, MD,
‡ Osman Ergun, MD,§ and Seda Sogukpinar Karaagac, MD*
Abstract: We aimed to determine histological damage in patients with varicocele by comparing the elasticity of their affected testes with that of their normal contralateral testes as well as normal testes of control subjects without varicocele using shear wave elastography (SWE). In total, 48 patients with varicocele (96 testes) and 52 control subjects (104 testes) were included in this study. Shear wave elastography values were measured in the longitudinal plane using an oval region of interest that covered as much of the testicular contours as possible. Fifty testes with varicocele were classified as group A, 46 normal con-tralateral testes of the same patients as group B, and 104 normal testes of control subjects as group C. The normal group C testes were ran-domly chosen from patients who had applied for ultrasonography for any reason and agreed to participate in the study. The testicular volume and SWE values were compared between these 3 groups. The average age of the patients was 28.45 years, and no significant difference in age was found between the 3 groups (P = 0.665). A significant difference in the testicular volume was found between groups A and C (P = 0.014). The SWE values were significantly higher in group A than in groups B and C (P < 0.001). No significant correlation was observed between the testicular volume and SWE values in any of the groups. Our results showed that SWE can be used as an effective technique to assess testic-ular stiffness in patients with varicocele to predict interstitial fibrosis and the severity of histological damage.
Key Words: shear wave elastography, varicocele, testis, ultrasonography
(Ultrasound Quarterly 2020;36: 64–68)
S
hear wave elastography (SWE) is a new sonographicimag-ing method that allows quantitative assessment (meter per second [m/s] and kilopascal [kPa]) of tissue stiffness. It gives in-formation about histological changes in the tissues and helps in differential diagnosis. The efficacy of SWE in evaluating the de-gree of fibrosis and stiffness caused by parenchymal damage
has been shown in various organs such as thyroid, breast, and
liver.1–7However, very few studies have focused on testicular
elasticity, and only 1 study has used SWE to evaluate testicular
damage and stiffness in patients with varicocele.8
A varicocele is the enlargement of pampiniform plexus veins, which are composed of lots of small vein networks in the spermatic cord. Scrotal varicocele is present in 15% of the
general population.9Varicocele is a well-known cause of
de-creased testicular function and is present in 35% to 44% of the men with primary infertility and in 45% to 81% of the men with
secondary infertility.10The retrograde flow in drainage veins in
varicocele causes venous stasis and an increase in temperature, leading to testicular parenchymal damage and consequently tes-ticular atrophy, and a decrease in testes-ticular function. In patho-logical examinations, the testicular damage due to varicocele manifests as a decrease in the seminiferous tubule diameter,
peritubular fibrosis, and Leydig cell atrophy.11A quantitative
evaluation of the degree of parenchymal fibrosis could reflect the parenchymal damage and decrease in testicular function caused by varicocele. Shear wave elastography can serve as an important tool in assessing and monitoring the progression of testicular fibrosis in varicocele.
In this study, to determine histological damage in patients with varicocele, we used SWE to measure the volume and elas-ticity of their affected testes and compared them with those of the normal contralateral testes of the same patients as well as the normal testes of control subjects without varicocele.
MATERIAL AND METHODS
This prospective controlled study was conducted at the Health Science University Konya Training and Research Hospi-tal from March 2017 to April 2018. The study was approved by the local research ethics committee of the Selçuk University Medical Faculty, Konya, Turkey. Written informed consent forms were obtained from all patients before ultrasonography (US) examination. All study procedures involving human par-ticipants were performed in accordance with the ethical stan-dards of the institution's national research committee and with the 1964 Helsinki Declaration and its later amendments or com-parable ethical standards.
No age restriction was applied when selecting patients for the study. Two patients were excluded from the study as SWE assessment could not be performed optimally in them because of excessive movement. In total, 48 patients with varicocele (96 testes) and 52 control subjects (104 testes) were included in the study. Two of the patients had bilateral varicocele. In
Received for publication August 6, 2018; accepted November 6, 2018. *Department of Radiology, University of Health Sciences, Konya Training and
Research Hospital;†Department of Family Medicine, Karatay Community Health Center;‡Department of Radiology, Selcuk University, Faculty of Medicine; and §Department of Urology, University of Health Sciences, Konya Training and Research Hospital, Konya, Turkey.
Address correspondence to: Hasan Erdogan, MD, Department of Radiology, University of Health Sciences, Konya Training and Research Hospital, 42090, Konya, Turkey (e‐mail: dr.hasanerdogan@gmail.com).
Copyright © 2019 Wolters Kluwer Health, Inc. All rights reserved. DOI: 10.1097/RUQ.0000000000000418
total, 50 testes with varicocele were classified as group A, their 46 normal contralateral testes were classified as group B, and 104 normal control testes were classified as group C. The group C testes were randomly chosen from the patients who had ap-plied for US for any reason, had no varicocele as per examina-tion, and agreed to participate in the study. Patients included in the study and classification of the testes are summarized in Table 1. The SWE values (m/s and kPa) and testicular volume were compared between the 3 groups.
All US and SWE examinations were performed by a sin-gle radiologist with 8 years of experience in US and 3 years of experience in SWE. All procedures were performed with the pa-tients in both supine and standing positions. All papa-tients underwent US, including color Doppler, and SWE examinations of the testes performed using a high-frequency (4- to 14-MHz)
linear array transducer (Toshiba Aplio 500; Toshiba Medical System Corporation, Tokyo, Japan). The location of varicocele (right or left testis) was determined by examining the testes using US and noted. All testes were measured in 3 dimensions (length
[L] width [W] height [H]), and the testicular volume was
then automatically calculated by the built-in software of the US
device using the formula L W H 0.523 (Fig. 1).
We used 2-dimensional SWE, which is the currently newest SWE method that uses acoustic radiation force. Some factors, such as cardiac motions, breathing, Valsalva maneuver, or patient and probe movements, can confound elastography measurements. In such a case, distorting propagation lines can
occur in SWE images.12 Therefore, we advised patients not
to breathe or move. In addition, in SWE examination, the transducer pressure on the skin should be similar to that in
reg-ular anatomical B-mode imaging.12 Therefore, we obtained
the elastography images of the testes by placing the US probe very lightly on the scrotum, without exerting any pressure. The values obtained from the acquisition images with motion arti-facts and distorting propagation lines of SWE were not consid-ered. Measurements were repeated in 15 patients who did not cooperate or moved during examination, and the repeated mea-surements provided ideal images. During the 5 seconds required to stabilize the SWE measurements, the images were captured and saved. Shear wave elastography images can be viewed using the following 3 display modes after freezing: speed mode (m/s),
TABLE 1. Details of the Testes Included in the Study According to Group Classification, Total No. Testes, and the Side Affected With Varicocele
Testes Group Total Number (%) Side (n) Testes with varicocele A 50 (25%) Left (48) Right (2) Opponent normal testes B 46 (23%)
Bilateral normal testes C 104 (52%) Total A + B + C 200 (100%)
FIGURE 1. Varicocele on the left testis of a 38-year-old patient. The largest pampiniform plexus vein diameter was 5.4 mm (A). In color Doppler US, venous reflux, which appears as an aliasing artifact, is observed during the Valsalva maneuver (B). Testes were measured in 3 dimensions, and the testicular volume was then calculated using the built-in software of the US device (C).
elasticity mode (kPa), and propagation (arrival time contour) mode. Tissue elasticity was indicated with a color range from dark blue (lowest stiffness) to red (highest stiffness), corresponding to 0 to 220 kPa (by default). Shear wave elastography values were measured in the longest longitudinal plane on a magnified view in all testes using an oval region of interest (ROI) that covered as much of the testicular contours as possible (Fig. 2). Shear wave elastography was used to obtain 3 measurements of each testis, the average of which was considered as the SWE value of the corresponding testis. This was thought to increase the ac-curacy of the numerical values obtained.
Statistical Analysis
All statistical analyses of the data were performed using the Statistical Package for Social Sciences Version 24 (IBM, Armonk, NY) software. Descriptive statistics were expressed as mean, standard deviation (SD), minimum to maximum values, frequency, and percentile. The Kolmogorov-Smirnov test was used to verify the normal distribution of the data. A parametric one-way analysis of variance (ANOVA) was performed to assess the testicular volume and m/s values because these values were normally distributed. Student' t test was used for their binary comparisons. The nonparametric Kruskal-Wallis test was per-formed to assess the age and kPa values because these values were not normally distributed. Mann-Whitney U test was used for their binary comparisons. A P value of less than 0.05 was con-sidered statistically significant with a 95% confidence level.
RESULTS
In total, 100 patients (200 testes) were enrolled in the study. Forty-eight of these patients had varicocele, of which 44 had varicocele in the left testis (91.6%), 2 had in the right tes-tis (4.2%), and 2 had bilaterally (4.2%), thus totaling to 50 testes with varicocele (group A) and 46 normal contralateral testes (group B). The remaining 52 patients with bilateral normal tes-tes constituted the control group (group C). Data are presented as mean ± SD. The mean age of the recruited patients was 28.45 ±10.48 years, and the mean ± SD testicular volume was 14.60 ± 4.26 mL. The mean age and testicular volume as well as SWE values of all 3 groups are listed in Table 2.
The mean ± age was 28.56 ± 8.95 years in group A, 27.52 ± 9.28 years in group B, and 28.79 ± 11.62 years in group
C, indicating no statistically significant difference in age be-tween the 3 groups (P = 0.665).
The mean ± SD testicular volumes in the 3 groups were as follows: 13.43 ± 4.64 mL in group A, 14.29 ± 3.82 mL in group B, and 15.27 ± 4.13 mL in group C. One-way ANOVA revealed a significant difference in the testicular volume between the 3 groups (P = 0.035, f = 3.424). Furthermore, 2-group compar-isons for the testicular volume performed using Student t test re-vealed a significant difference between groups A and C (P = 0.014), but no significant difference was found between groups A and B (P = 0.329) or groups B and C (P = 0.175).
The mean ± SD SWE values were 1.83 ± 0.34 m/s and 12.61 ± 6.23 kPa in group A, 1.59 ± 0.24 m/s and 9.23 ± 3.23 kPa in group B, and 1.62 ± 0.31 m/s and 9.42 ± 4.30 kPa in group C. The mean SWE values were higher in group A than in groups B and C. One-way ANOVA revealed a significant dif-ference in the m/s values between the 3 groups (P = 0.001, f = 9.250). Two-group comparisons for the m/s values using Student t test revealed a significant difference between groups A and B as well as groups A and C (both, P = 0.001), but no sig-nificant difference was found between groups B and C (P = 0.580). Furthermore, Kruskal-Wallis test revealed a signif-icant difference in the kPa values between the 3 groups (P = 0.001). Two-group comparisons for the kPa values using Mann-Whitney U test revealed a significant difference between groups A and B as well as groups A and C (both, P = 0.001), but no significant difference was found between groups B and C (P = 0.934).
Furthermore, no significant correlation was found between the testicular volume and m/s and kPa values in the groups (for m/s values: P = 0.566, 0.333, and 0.917 in groups A, B, and C, respectively; for kPa values: P = 0.934, 0.130, and 0.741 in groups A, B, and C, respectively).
FIGURE 2. Varicocele on the left testis of a 38-year-old patient. Shear wave elastography images can be viewed using 3 display modes after freezing: propagation mode (A), speed mode (m/s) (B), and elasticity mode (kPa) (C). Quantitative elasticity measurements were obtained in the longest longitudinal plane on a magnified view using an oval ROI that covered as much of the testicular contours as possible. The elasticity values were 1.51 m/s (B) and 7.5 kPa (C) in this patient.
TABLE 2. Mean Age, Testicular Volume, and SWE Values of the Testes According to the Groups
Mean ± SD
Group Age, y Volume, mL m/s kPa A 28.56 ± 8.95 13.43 ± 4.64 1.83 ± 0.34 12.61 ± 6.23 B 27.52 ± 9.28 14.29 ± 3.82 1.59 ± 0.24 9.23 ± 3.23 C 28.79 ± 11.62 15.27 ± 4.13 1.62 ± 0.31 9.42 ± 4.30 A + B + C 28.45 ± 10.48 14.60 ± 4.26 1.67 ± 0.32 10.17 ± 4.84
DISCUSSION
Varicocele is characterized by retrograde blood flow of tes-ticular veins and abnormal folding and dilatation of pampiniform
plexus.13 Wide vein diameter, retrograde venous flow during
Valsalva maneuver, and venous curling are the 3 sonographic di-agnostic criteria for varicocele. Of these 3, the first 2 criteria were widely used for varicocele diagnosis. The suggested cut-off value
for the minimum vein diameter is 2 to 3 mm.13,14Scrotal
var-icocele is present in 15% of the general population,9with left
side occurrence observed in 80% to 90%, right side occurrence in 1% to 7%, and bilateral occurrence in 2% to 20% of the
af-fected population.15Varicocele is the most common treatable
cause of male infertility.9One study has shown remarkable
im-provement in spermogram parameters and conception rates
af-ter varicocele treatment.16
Shear wave elastography is a new noninvasive imaging technology that provides information about histological changes in tissues. It allows valuable quantitative assessment of tissue
stiffness and is very helpful in differential diagnosis.1–7 Using
SWE, stiffness can be evaluated in both focal lesions and diffuse
diseases by marking the relevant area (by putting ROI).12The
basic principles of SWE are compression of the tissue of interest and application of a US probe that automatically produces an acoustic push pulse to generate shear waves. Tissue stiffness is then determined based on the detected shear velocity. The un-derlying principle is that shear wave tissue propagation velocity depends on tissue consistency; propagation is slower through softer tissues (normal testes) and faster through harder tissues (stiffer testes). The shear wave speed is measured in both m/s
and kPa.2,12The quantitative elasticity values measured in kPa
and m/s show good diagnostic performance. However, in 1 study, the specificity of the SD and area under the receiver operating characteristic curve of the lesion measured in kPa were found
to be significantly higher than those measured in m/s.17Because
both the kPa and m/s SWE values could be obtained performing 1 examination, we measured both in our study. Recent studies have demonstrated the efficacy of SWE in predicting the degree
of fibrosis in several organs.1–7Shear wave elastography is
fre-quently used for diagnosing testicular lesions and diseases. In some studies, testicular tumor, torsion, and infarct as well as
undescended testes were evaluated using SWE.18–21However,
only 1 study has used SWE for evaluating varicocele.8That
study evaluated the correlation of hormonal levels and semen analysis results with SWE values in infertile patients with var-icocele, but the testes with varicocele were not compared with normal contralateral testes or the testes of healthy individuals. In varicocele, the retrograde flow in drainage veins causes venous stasis and an increase in testicular temperature, resulting in testicular parenchymal damage, testicular atrophy, and a
de-crease in testicular function.10,15In our study, no statistically
significant difference was found between the 3 groups (A, B, and C) in terms of age. However, a significant difference was observed in the testicular volumes between groups A and C but not between groups A and B. In addition, no significant cor-relation was observed between the SWE values (m/s and kPa) and the testicular volume. These findings confirmed that the tes-ticular volume tends to decrease in the testes with varicocele compared with normal testes, but this decrease is not associated with the degree of fibrosis, as indicated by the absence of
correlation between changes in the SWE values and testicular volumes in this study. Thus, the testicular volume is not a reliable parameter for reflecting the degree of parenchymal damage. This result may be due to the limited group size. The results of studies in the literature are contradictory regarding whether the testicular volume is a useful parameter for predicting the degree of
intersti-tial fibrosis.22–25High SWE values may be a more reliable
pa-rameter than the testicular volume for reflecting interstitial fibrosis and thus the severity of damage.
In pathological studies, findings such as a decreased sem-iniferous tubule diameter, peritubular fibrosis, and Leydig cell
atrophy have been reported in testes with varicocele.11
Testicu-lar biopsy can be performed to assess the histological features of parenchymal damage, but it is not a preferred method because it is invasive. In addition, spermogram can be used to indirectly
reflect parenchymal damage.26In our study, significant
differ-ence was observed in SWE values between testes with varico-cele (group A), normal contralateral testes of the same patients (group B), and the testes of healthy individuals (group C). The SWE values (m/s and kPa) of group A were significantly higher than those of groups B and C. These findings confirmed that the SWE values tend to increase in parallel with increasing degree of fibrosis. Therefore, SWE is a reliable technique for quantita-tively measuring the changes in testicular tissue stiffness in pa-tients with varicocele. The potential role of SWE in measuring testicular tissue stiffness has also been demonstrated by
histo-logical examination on rabbits in a previous study.27In addition,
SWE can be used as a complementary tool for evaluating and monitoring the extent of damage, the progression of damage, or regression of damage after surgery. Although our findings were not confirmed by histopathological examination, SWE was found to be a useful technique in assessing testicular dam-age in varicocele. However, further studies using a larger sam-ple size are required to confirm the efficacy of SWE technique in routine varicocele evaluation.
Several studies have evaluated testes using SWE.18–21,27
Similar to the studies conducted on other organs, those con-ducted on testes also performed SWE measurements in limited areas with a constant small circle or square ROI. However, a standard area for evaluation was not established in these studies. Shear wave elastography values may differ in different parts of the same organ. Therefore, in this study, we used oval ROI cov-ering the entire testicular parenchyma because we hypothesized that it would increase the reliability of SWE measurements. Similarly, in some studies, to overcome this limitation, SWE values were obtained by manually drawing the entire testicular parenchyma with a free ROI in the longest axis in the
longitudi-nal plane.20,28However, it is time-consuming in daily clinical
practice to manually draw the testicular parenchyma using a free ROI. Therefore, we used an oval ROI for both performing the examination in a shorter time and obtaining SWE measurements in the longitudinal plane of the testicular parenchyma. We be-lieve that the method used for SWE measurements in our study is rapid and can be used as a reliable tool for diagnosis and follow-up in daily clinical practice to assess the severity of dam-age in testes with varicocele. Therefore, studies assessing the ef-fect of different types of ROI on SWE measurements are needed. Our study had some limitations. First, we could not per-form histopathological evaluation of the testes. However, it is
not quite possible to conduct such evaluations because of the na-ture of varicocele operations. Second, although the sample size
was greater in our study than in the previous study,8 further
studies using a larger sample size are needed to confirm the ef-ficacy of our SWE technique. Third, only 1 operator performed all of the examinations, so we could not evaluate interobserver variability. Lastly, the SWE measurements were taken in the en-tire testicular parenchyma included in the examination area in a single section in the longitudinal plane. We believe that if the measurements are taken in more than 1 section, the reliability of the SWE values may increase.
In conclusion, the results of our study suggest that SWE can be used as an effective technique to assess the testes with varicocele to predict interstitial fibrosis and monitor the severity of parenchymal damage. No correlation exists between the tes-ticular volume and the SWE values. Therefore, the testes-ticular volume is not a reliable parameter for reflecting the degree of parenchymal damage. Further studies with a larger number of patients are needed to confirm the efficacy of SWE in routine varicocele evaluation.
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