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World J Urol (2011) 29:645–650

DOI 10.1007/s00345-011-0701-4

TOPIC PAPER

Color Doppler ultrasound imaging in varicoceles: is the venous


diameter sufficient for predicting clinical and subclinical
varicocele?
A. Pilatz • B. Altinkilic • E. Köhler •

M. Marconi • W. Weidner

Received: 27 February 2011 / Accepted: 10 May 2011 / Published online: 24 May 2011
Ó Springer-Verlag 2011

Abstract compared with all other grades (P \ 0.001). There were no


Purpose Investigating the diagnostic value of color side-related differences when comparing identical varico-
Doppler ultrasound for defining the varicocele grade cele grades (in all cases P [ 0.1). Venous diameters above
according to WHO criteria. 2.45 mm in rest (sensitivity 84%, specificity 81%) or
Methods A total of 217 men (129 with clinical varicocele 2.95 mm during Valsalva (sensitivity 84%, specificity
and 88 without clinical varicocele) were investigated by 84%) predicted the presence of a clinical varicocele.
physical examination and color Doppler ultrasound and Conclusions Our findings support the hypothesis that
categorized according to WHO varicocele criteria (0, clinical varicoceles can be predicted with high accuracy
subclinical, I, II, and III). Diameter and reflux of the largest based only on the diameter of testicular veins using cut-
vein in the pampiniform plexus were measured bilaterally point values of [2.45 mm in rest or [2.95 mm during
with the patient in the supine position in rest and during the Valsalva maneuver in the supine position.
Valsalva maneuver. To assess the possibility of differen-
tiating varicocele grade by venous diameter, optimal cut-point Keywords Varicocele  Color Doppler ultrasound 
values were determined by receiver-operator characteristic Infertility  Venous diameter
(ROC) analysis.
Results With increased varicocele grade, a larger vein Abbreviations
diameter was more significant in rest and during Valsalva CDU Color Doppler ultrasound
(in all cases P \ 0.05), except between grade I and grade ROC Receiver-operator characteristic
II. Retrograde peak flow velocities were similar in every
group (in all cases P [ 0.1). Only grade III varicoceles
demonstrated significantly increased peak flow values

Introduction
A. Pilatz, B. Altinkilic contributed in equal parts.
Varicoceles are abnormal dilations of the pampiniform
M. Marconi was a fellow in ‘‘Clinical Andrology’’ at the Department
of Urology in Giessen (2007–2008), Scholarship MIDEPLAN Chile. plexus. This condition was already known by A. Celsus
(first century AD), who gave a detailed report of a vari-
A. Pilatz (&)  B. Altinkilic  E. Köhler  M. Marconi  cocele and its operative therapy [1].
W. Weidner Varicoceles are found in 20–40% of infertile men, but in
Department of Urology, Pediatric Urology and Andrology,
University Hospital Giessen and Marburg GmbH—Giessen, only 15% of the general population [2, 3]. Although it is
Justus-Liebig University Giessen, Rudolf-Buchheim-Strasse 7, widely accepted that idiopathic varicoceles are mainly
35385 Giessen, Germany evident on the left side [3], some authors propose a bilat-
e-mail: adrian.pilatz@chiru.med.uni-giessen.de eral disease [4, 5]. The direct association between varico-
M. Marconi cele and male infertility is unknown, but a negative impact
Urology Unit, Complejo Hospitalario San Jose, Santiago, Chile on semen and testicular volume is well documented [2].

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However, a substantial number of men with a clinical accordance with the WHO: 0 (no varicocele), grade I
varicocele have no fertility problems [2]. Although vari- (palpable during Valsalva maneuver), grade II (palpable
cocele repair is discussed controversially [6], current data without Valsalva maneuver), and grade III (visible through
support the idea that therapy of clinical varicoceles does the scrotal skin). Subclinical varicocele was classified as
have a beneficial effect on improving seminal parameters non-palpable, but with retrograde reflux under Valsalva
as well as assisting infertile couples to achieve pregnancy maneuver as visualized using CDU [9].
spontaneously [7, 8]. The study was carried out by two experienced investi-
The clinical diagnosis of varicocele is made by physical gators (A.P., E.K.) to avoid bias in the diagnosis of vari-
examination in a warm room [9], but the specificity of this cocele and mistakes in interpreting the CDU findings.
assessment is only about 70% [3, 10]. In contrast, color High-frequency ultrasound with color Doppler imaging
Doppler ultrasound has a sensitivity of 97% and a speci- was performed using a 7.5 MHz transducer (SonoAce
ficity of 94% [10]. Due to its noninvasiveness, color 8800, Sonoace Deutschland GmbH, Marl, Germany).
Doppler ultrasound has replaced the former gold standard During the investigation, diameter and reflux of the largest
of venography [11]. Although men with impaired fertility vein in the pampiniform plexus were measured bilaterally
are often investigated for the presence of a varicocele by with the patient in the supine position. Basal vein diameter
scrotal ultrasound, no generally accepted criteria are and continuous spontaneous reflux were obtained when the
available. This is because several modalities have been patient was relaxed. Maximum vein diameter and peak
used for ultrasound-based diagnosis. In this connection, retrograde flow were evaluated during the Valsalva
various possibilities have been investigated: measuring maneuver (Fig. 1 a–d). At least three separate measure-
venous diameters in an upright [12–14] or supine position ments of each variable were made and subsequently
[15, 16], measuring only venous diameters [14, 17], and averaged.
measuring venous diameter and retrograde flow [3, 18–20]. Vein diameters and reflux in the different groups were
Other studies have involved heterogeneous populations compared with non-parametric tests for unpaired samples.
comprising healthy controls and infertile patients with Differences in vein diameter before and during Valsalva
clinical, subclinical or no varicoceles, resulting in different maneuver were compared with non-parametric test for
cut-points for venous diameters and retrograde peak flow paired samples. The cutoff points, sensitivity, and speci-
[3, 12–20]. ficity for vein diameters were determined by receiver-
The purpose of this study was to determine whether operator characteristic (ROC) analysis. The ‘‘optimal’’
specific scrotal color Doppler ultrasound (CDU) parame- operating point of the ROC curve was chosen as the value
ters (basal venous diameter, maximum venous diameter that produced the point closest to 100% sensitivity and
during Valsalva maneuver, continuous spontaneous reflux, 100% specificity. The results were expressed as medians. A
peak retrograde flow) can be used to predict varicocele value of P \ 0.05 was considered statistically significant.
grade according to WHO criteria in patients with and Statistical analyses were performed using PASW Statistics
without clinical varicocele. 18 for Windows (SPSS GmbH Software, Munich,
Germany).

Patients and methods


Results
After approval of the institutional review board, we con-
ducted a prospective study from 2004 to 2010 on color A total of 434 testicles in 217 men were examined and
Doppler ultrasound in 129 patients with clinical varicocele scanned by color Doppler ultrasound. In 258 testicular
(median age 30 years, range 12–62 years) and 88 healthy units from 129 patients (with clinical varicocele), 146
controls without clinical varicocele (median age 35 years, clinical varicoceles (grade I: 11 right, 52 left; grade II: 7
range 19–61 years). The study excluded men who had right, 42 left; grade III: 1 right, 33 left) and 26 subclinical
undergone previous varicocele repair, scrotal surgery, or varicoceles (25 right, 1 left) were recorded. A subclinical
hernia repair, men who had suffered a symptomatic vari- varicocele was identified in 18 out of 176 testicular units (8
cocele (e.g., renal cell cancer), men with a history of uro- right and 10 left) from 88 controls (without clinical vari-
genital infection, and men with single testes. Controls were cocele). In all subclinical and clinical varicoceles, a ret-
enrolled during routine prevention care in our outpatient rograde flow was observed during the Valsalva maneuver.
department. The median basal vein diameter in a relaxed supine
The presence of a clinical varicocele was determined by position was 1.6 mm (grade 0), 2.2 mm (subclinical),
palpation and observation in the standing position before 3.0 mm (grade I), 2.8 mm (grade II), and 2.9 mm (grade
and during the Valsalva maneuver. Classification was in III) on the right and 1.4 mm (grade 0), 1.8 mm

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World J Urol (2011) 29:645–650 647

Fig. 1 a B-scan of a grade III


varicocele in relaxed supine
position. b B-scan of the same
varicocele during Valsalva
maneuver. c Color Doppler
ultrasound of a grade III
varicocele depicting continuous
spontaneous reflux. d Color
Doppler ultrasound of a grade
III varicocele during Valsalva
maneuver

(subclinical), 3.0 mm (grade I), 3.2 mm (grade II), and discriminating between testicular units without clinical
3.4 mm (grade III) on the left side, respectively. There varicocele and with clinical varicocele in the relaxed
were no side-related differences regarding identical grades supine position was 2.45 mm (sensitivity 84%, specificity
(in each case P [ 0.1). With increasing varicocele grade, a 81%). During Valsalva maneuver, the optimal cutoff point
larger basal vein diameter became significant (in each case was 2.95 mm (sensitivity 84%, specificity 84%) in the
P \ 0.05), except between grade I and grade II (Fig. 2a). same testicular units. Discriminating between testicular
During Valsalva maneuver, a median increase of units without varicocele and with subclinical varicocele on
0.3 mm in all vein diameters compared to baseline was the basis of venous diameters resulted in less favorable
recorded (P \ 0.001). Median maximum vein diameter results. The area under the ROC curve was 0.655 for basal
was 1.8 mm (grade 0), 2.7 mm (subclinical), 3.7 mm venous diameter, 0.673 for maximum venous diameter, and
(grade I), 4.1 mm (grade II), and 3.4 mm (grade III) on the 0.602 for the diameter difference of both (Fig. 3b). All
right and 1.7 mm (grade 0), 2.2 mm (subclinical), 3.65 mm possible cutoff points showed sensitivity and specificity
(grade I), 3.75 mm (grade II), and 4.7 mm (grade III) on both below 70%. When calculating side-specific cutoff
the left side, respectively. Again, there were no side-related diameters, no advantage was found.
differences when comparing identical grades (in each case In 146 clinical grade I-III varicoceles, 17 cases with a
P [ 0.3), but with increasing varicocele grade, a larger continuous spontaneous reflux were found (11.6%). Due to
maximum vein diameter was significant (in each case the low number of cases, an association between varicocele
P \ 0.05), except between grade I and grade II (Fig. 2b). grade and reflux altitude could not be demonstrated.
We assessed the ability of the basal venous diameter, the Median retrograde peak flow was 8 cm/s (subclinical),
maximum venous diameter during Valsalva maneuver, and 7 cm/s (grade I), 12 cm/s (grade II), and 13.95 cm/s (grade
the arithmetic difference of both in order to distinguish III) on the right and 7 cm/s (subclinical), 11 cm/s (grade I),
testicular units with no clinical varicocele from those with 11 cm/s (grade II), and 19.85 cm/s (grade III) on the left
clinical varicocele. The area under the ROC curve was side, respectively (Fig. 4). Identical grades showed similar
0.883 for basal venous diameter and 0.904 for maximum retrograde peak flow values when comparing both sides (in
venous diameter, indicating this value to be a good clas- each case P [ 0.1). While subclinical, grade I, and grade II
sifier. On the other hand, the area under the ROC curve was had similar peak flow velocities (in each case P [ 0.1),
only 0.779 for the diameter difference before and during grade III varicoceles demonstrated significantly increased
Valsalva maneuver (Fig. 3a). The optimal cutoff point for peak flow values (P \ 0.001).

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Fig. 2 Vein diameters subject to varicocele grade and based on the Fig. 3 ROC curve analysis for predicting a clinical varicocele and
side investigated. a is before and b is during Valsalva maneuver. No b subclinical varicocele by venous diameters in rest, during Valsalva
side-related difference in vein diameter (in each case P [ 0.1). maneuver and using the arithmetic difference of both
Significant increase in venous diameter to the next higher WHO
group (in each case P \ 0.05), except between grade I and grade II. ultrasound, this method is recommended in cases of doubt
Box and whisker plots display median values, quartiles, and and for confirming diagnosis [10, 11, 21]. Color Doppler
(o) outliers ultrasound detects a varicocele either by measuring
augmented scrotal vein size or by demonstrating blood
Discussion refluxing through the pampiniform plexus during the
Valsalva maneuver. The measurement of retrograde peak
Varicocele is the most common cause of infertility in men flow creates a possibility to detect further subclinical
[11]. It is accompanied by reflux, causing dilation in the varicoceles [9].
pampiniform plexus. This condition is routinely used as a Our prospective study sought to determine whether
diagnostic tool in detecting varicocele by physical exami- color Doppler ultrasound can predict the grade of sub-
nation [9]. Detection of a varicocele by palpation is closely clinical and clinical varicocele. In contrast to others [5, 14,
associated with increased vein diameter. In this context, 15, 17], we evaluated a large group of 217 men: 129 suf-
Hoekstra and coworkers noted that veins smaller than fering from clinical varicocele and 88 without clinical
2.5 mm are never palpable, while scrotal veins with varicocele, who served as controls. In order to obtain
diameters larger than 3.5 mm are always palpable [12]. complete evaluation of the status in the spermatic veins,
Although clinical diagnosis of varicocele can be made physical examination was performed in the standing posi-
directly by physical examination, the specificity of this tion, and sonographic findings were noted in the supine
assessment is only about 70% [3, 10]. Due to the high position in rest and during Valsalva maneuver. Further-
sensitivity (97%) and specificity (94%) of color Doppler more, all scanned testicular units were analyzed separately

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Interestingly, Hussein discovered that in veins larger than


2.5 mm, reflux can be found in 85.6% of the cases [19].
These data are absolutely in accordance with our results
and reflect the importance of the 2.45-mm vein diameter
cutoff in rest for predicting clinical varicocele. During
Valsalva maneuver, the optimal cutoff point climbed to
2.95 mm (sensitivity 84%, specificity 84%). Several cutoff
values for venous diameters (2.0, 2.5, and 3.0 mm) have
been proposed [15, 19, 20], but to our knowledge, they
have never been determined by ROC analysis. Our results
clearly indicate that, in many cases, Doppler evaluation can
be omitted, because a B-scan of vein diameters in rest or
during Valsalva maneuver predicts clinical varicocele with
high accuracy.
However, the diagnosis of subclinical varicocele based
only on the diameter of the veins is characterized by a high
Fig. 4 Retrograde peak flow subject to varicocele grade and based on number of false positives and negatives (sensitivity and
the side investigated. No side-related difference in peak flow (in each
case P [ 0.1). Only grade III demonstrated significantly increased specificity each below 70%). Thus, to detect subclinical
peak flow compared to other groups (#P \ 0.001). Box and whisker varicocele, color Doppler ultrasound is mandatory. Here, our
plots display median values, quartiles, and (o) outliers findings are in accordance with the results of other authors [3,
13, 18, 20]. Moreover, it remains debatable whether sub-
on both sides, including varicocele grade before and during clinical varicocele is clinically relevant at all [6, 18].
Valsalva maneuver. Unfortunately, some other authors Although the peak retrograde flow increased with higher
mixed up different grades [12, 14, 16] or did not specify if varicocele grades, we detected a significant difference only
the results were found in an upright or a supine position, in in patients with grade III. In all other groups, peak flow
rest or during Valsalva [15, 18, 20]. This complicates any velocities were comparable at about 9 cm/s, as found by
proper interpretation. Furthermore, the use of primarily others [13]. This makes the peak flow velocities useless for
pooled data for venous diameters of different testicular differentiating between grades. Nevertheless, retrograde
sides [13, 16, 20] is questionable because of the varying peak flow velocities might be of importance for predicting
venous drainage. Nevertheless, our current results clearly progression or a new onset of testicular asymmetry in
show that venous diameters and retrograde peak flow adolescents [22].
velocities do not differ between sides.
The main goal of our study was to consider the impor-
tance of venous diameter as a predictor of varicocele grade. Conclusions
The investigations showed that venous diameters in a
relaxed supine position and during Valsalva maneuver Our data support the hypothesis that by means of color
increased significantly from a lower to the next higher Doppler ultrasound, clinical varicoceles can be predicted
grade on both sides. Only grades I and II did not differ with high accuracy (sensitivity [80%, specificity [80%)
significantly. This increase in venous diameter is in based only on the diameter of testicular veins using cut-
accordance with the data of other authors [3, 20]. However, point values of 2.45 mm in rest or 2.95 mm during the
in contrast to our findings, some studies noted a pro- Valsalva maneuver in the supine position. However, sub-
nounced overlap in venous diameters, making it impossible clinical varicoceles cannot be reliably differentiated from
to differentiate properly between subclinical, grade I, and testicular units without varicocele. The venous diameter
no varicoceles [3, 13, 18, 20]. difference before and during Valsalva as well as peak
Interestingly, the caliber increase of venous diameter in flow velocities are unsuitable for distinguishing between
the relaxed position in comparison with the Valsalva varicocele grades.
maneuver is only slight, with a median of 0.3 mm, and not
useful in differentiating varicocele grade. Here, our results Conflict of interest The present authors have no conflict of interest.
are in accordance with previous studies [14, 17].
Using ROC analysis, we identified the optimal cutoff References
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