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0022-5347 /94/1516-1535$03.

00/0
TaE JOURNAL OF URO!,OGY Vol.
Copyright@ 1994 by AMERJCAN UROLOGICAL ASSOCIATION, INC.

THE INCIDENCE OF VARICOCELES IN THE GENERAL


POPULATION WHEN EVALUATED BY PHYSICAL EXAMINATION 1

GRAY SCALE SONOGRAPHY AND COLOR DOPPLER SONOGRAPHY


RANDALL B. MEACHAM, RONALD R TOWNSEND, DANA RADEMACHER AND JULIA A. DROSE
From the Division of Urology, Department of Surgery and Division of Ultrasound, Department of Radiology, University of Colorado Health
Sciences Center, Denver, Colorado and Department of Urology, University of California, Davis, California

ABSTRACT
The association between male subfertility and varicocele has long been recognized. Physical
examination is the most widely used method for detecting varicoceles but other techniques may be
more sensitive. Color Doppler sonography has the theoretical advantage of allowing direct demon-
stration of reversed flow in the testicular veins. The frequency of detection of reversed flow by color
Doppler ultrasound in a normal population is, however, unknown. We evaluated 34 asymptomatic
young men with physical examination, standard scrotal sonography and color Doppler evaluation
of the scrotal veins. Findings were correlated with semen analysis. Of the subjects 15% had
varicoceles by physical examination and 18% by scrotal sonography, while 35% had retrograde flow
by color Doppler evaluation. The majority of men in this population did not exhibit retrograde flow
within the gonadal veins when evaluated by color Doppler sonography. The physiological significance
of retrograde flow, however, remains to be defined.
KEY WORDS: varicocele, ultrasonography, Doppler ultrasound, infertility

The relationship between varicocele and male subfertility ommended its use to direct more invasive testing and treat-
has been recognized since the late 19th century. 1 In 1962 ment.
Charney discussed the effect of varicocele on male fertility and As highly sensitive diagnostic modalities, such as color
reported improvement in semen quality following correction of Doppler sonography, are developed and refined, it will certainly
this lesion. 2 Soon thereafter, MacLeod described specific semen become easier to detect scrotal varicosities that are too subtle
abnormalities associated with the presence of varicocele. He to identify on physical examination. While this will afford the
observed that men with varicoceles exhibited decreased sperm practitioner greater diagnostic information, the application of
concentration, decreased sperm motility and an increased num- these technologies may still be confusing. Criteria must be
ber of sperm showing abnormal morphology. 3 In 1970 Dubin developed to differentiate which veins are pathological and
and Amelar reiterated the association between varicocele and which are simply normal components of the testicular vascu-
male subfertility but concluded that the size of the varicocele lature. An issue that has not been adequately addressed is the
does not correlate with its impact on semen quality. 4 In con- prevalence of varicoceles detectable by highly sensitive tech-
trast, in 1993 Steckel et al presented data suggesting that large niques, such as gray scale and color Doppler sonography, in the
varicoceles are more detrimental to semen quality than are general population. If such lesions prove to be highly prevalent,
small varicoceles. 5 In 1955 Tulloch stimulated interest in vari- this may suggest that these modalities are excessively sensitive.
cocele repair for the treatment of male infertility when he Therefore, improper interpretation of such studies might lead
reported a pregnancy in the partner of a previously azoospermic to unwarranted surgery. We investigate the prevalence of var-
patient following bilateral varicocele ligation. 6 Since then, nu- icocele in the normal population using color Doppler sonogra-
merous investigators have reported improvement in semen phy. Findings are correlated with physical examination, gray
quality following varicocele correction. 7 scale sonography and semen analysis.
Given the association between varicocele and male subfertil-
MATERIALS AND METHODS
ity, as well as the potential for enhanced fertility following
varicocele repair, considerable attention has been devoted to All subjects volunteered for participation in this study. The
improving techniques for the diagnosis of this lesion. The most study was approved by the Institutional Revie,N Board for
common method of identifying varicocele is physical examina- research involving human subjects at the University of Colo-
tion. This technique is convenient, inexpensive and noninva- rado Health Sciences Center. Participation was solicited using
sive. Physical examination, however, is somewhat subjective publicly circulated notices. Inclusion in the study required a
and is dependent on the experience of the examining physician. history negative for genitourinary trauma or surgery as well as
Additionally, it has been suggested that small varicoceles not the absence of previously identified fertility problems. Of 34
detectable by physical examination alone (subclinical varico- subjects 18 to 40 years old (mean age 28.4 years) accepted for
celes) may have a role in subfertility and, therefore, merit study 7 had previously fathered children.
correction. 8 • 9 All individuals submitted 2 semen specimens that were eval-
Recently, attention has been focused on the use of color uated for ejaculate volume, sperm concentration, motility, for-
ward progression and morphology as well as semen viscosity
Doppler sonography in the detection of varicocele. In 1991
and semen leukocyte content. To standardize the results of
Petros et al described the use of this modality in the detection
semen analysis, subjects were required to collect all semen
of varicocele, and compared it to physical examination and
specimens 2 to 5 days following the last ejaculation. Semen
venography. 10 Usingvenography as the reference standard, they
samples were evaluated in accordance with World Health Or-
found color Doppler sonography to be more sensitive than
ganization standards. 11 Normal values were defined as volume
physical examination in the detection of varicoceles and rec- 1.5 to 5 cc, concentration greater than 20 million per ml. and
Accepted for publication October 22, 1993. motility 50% or greater as well as 50% or more of sperm showing
1535
1536 INCIDENCE OF VARICOCELES IN GENERAL POPULATION

normal morpholgoy. A subject was considered to have normal


semen quality if both specimens were normal or if 1 specimen
was entirely normal and the other specimen had only 1 param-
eter that was subnormal. Laboratory personnel performing
semen analyses were unaware of the results of physical exami-
nation or sonographic evaluation.
All subjects underwent physical examination performed by 1
urologist. The examining physician was unaware of the results
of semen analysis or sonographic evaluation. Scrotal examina-
tion was performed with the patient in the standing position
before and during Valsalva's maneuver. Subjects were assessed
for the presence of varicocele as well as testicular size and
consistency. All varicoceles identified at physical examination
were classified as grade 1 (palpable only during Valsalva's
maneuver), grade 2 (palpable without Valsalva's maneuver) or
grade 3 (visible without the need for palpation).
Scrotal sonography was performed by a single radiologist on
all subjects using an Acuson 128 real-time scanner. A linear 5
MHz. transducer was used for all examinations. Testicular
length, width and anterior-posterior dimension were measured.
All participants were required to stand for 2 minutes before
beginning scanning in the upright position to increase hydro-
static pressure within the veins. The number of veins and the FIG. 2. Color Doppler iinage demonstrates retrograde flow, in blue
maximum diameter of the largest vein were evaluated at rest (away from transducer), within dilated vein.
and during Valsalva's maneuver with the patient in the supine
and standing positions. Color Doppler sonography was used to
Macintosht computer. A p value of <0.05 was considered
detect the presence and direction of venous flow at rest and
statistically significant.
following Valsalva's maneuver. A standard color map was used
that arbitrarily assigned blue to retrograde flow (away from the
RESULTS
transducer) and red to antegrade flow (towards the transducer)
within the testicular veins. A varicocele was considered to be Among 8 subjects (24%) with subnormal semen quality 3 had
present by gray scale evaluation if 2 or more veins could be varicoceles by physical examination, 2 by gray scale sonography
identified, with at least 1 vein having a diameter of 3 mm. or and 4 by color Doppler sonography. Two subjects with de-
greater (fig. 1). A varicocele was considered to be present by creased semen quality were not identified as having a varicocele
color Doppler sonography if retrograde flow was identified by any of the 3 diagnostic methods.
within the pampiniform plexus spontaneously and/or during Overall, 5 subjects (15%) had a varicocele by physical ex-
Valsalva's maneuver (fig. 2). The physician performing sono- amination: 2 had unilateral (left) and 3 had bilateral varico-
graphic evaluation was unaware of the results of physical celes. All 6 subjects (18%) who had a varicocele by gray scale
examination or semen analysis. scrotal sonography were judged to have unilateral left lesions
Contingency table analysis was performed to compare the by sonographic criteria. Six subjects had a vein with a diameter
efficacy of all diagnostic studies with the outcome variable of of greater than 3 mm. but on closer examination they were
semen analysis. Fisher's exact test and chi-square statistics believed to have only 1 identifiable vein. Therefore, these
were examined using Statview II* statistical software and a individuals were not classified as having a varicocele by gray
scale sonography.
* Avacus Concepts, Berkeley, California. When evalu.ated with color Doppler sonography, 12 subjects
(35%) had retrograde flow within the pampiniform plexus
consistent with a varicocele: 6 only on the left side, 2 only on
the right side and 4 bilaterally. A summary of these results is
presented in the table. Among the 26 subjects with normal
semen quality 2 (8%) had a varicocele by physical examination,
4 (15%) by gray scale evaluation and 8 (31 %) by color Doppler
sonography.
Among the 5 subjects with a varicocele on physical exami-
nation, 3 also had a varicocele by gray scale sonography, while
4 had retrograde venous flow by color Doppler sonography.
Although physical examination is a standard technique for
detecting varicocele, factors such as a bulky spermatic cord or
thick scrotal skin may make physical examination difficult. Of
the 2 subjects believed to have a varicocele by physical exami-
nation but not by sonographic criteria 1 had a single 2 mm.
vein with retrograde flow and 1 did not have any veins greater
than 2 mm. in diameter. Three of the patients identified as
having varicoceles by gray scale sonography also had a positive
physical examination and 4 had retrograde venous flow iden-
tified by color Doppler sonography. Of the 12 subjects with
retrograde venous flow on color Doppler sonography 3 also had
a varicocele on physical examination, while 4 had varicoceles
by gray scale sonographic criteria. Six of the subjects (50%)
FIG. 1. Longitudinal image of lower spermatic cord, superior to left
testis. Hypoechoic linear structure (arrow) represents dilated vein. t Apple Products, Inc., Cupertino, California.
iNCiDEJ\lCE OF VARICOCELES GENERAL POPULAT10I'"'<l 1537
Results of evaluations among individuals noted to have uaricoceles by invasive and, ,nm•A.,,M is not appropriate for screen-
either color Doppler sonography, gray scale scmography or physical ing. Additionally, since invasive nature of venography pre-
examination cludes its use for evaluation of fertile subjects for research
Varicocele purposes, it is not known how commonly retrograde flow within
Pt. No. the gonadal vein occurs in the general population. Thus, it is
Color Gray Physical
Doppler Scale Examination
not clear which individuals with valvular incompetence are at
risk for subfertility.
1 Rt.
2 Lt.
Gray scale sonography has been proposed as a sensitive yet
3 Lt. noninvasive method of detecting varicoceles. In 1986 McClure
4* Bilat. and Hricak reported the evaluation of 50 subfertile men using
5 Lt. this technique. 8 They noted that 25 of these patients (50%) had
6 Bilat. Lt. Bilat.
7*· t Lt.
a varicocele on physical examination, while 34 (68%) had a
8* Lt. Lt. varicocele on sonographic evaluation. Among a control group
9 Lt. Lt. Bilat. of 25 patients evaluated before vasectomy 4 (16%) had a vari-
lOt Lt. Lt. Lt. cocele on physical examination compared to 8 (32%) on scrotal
11 Rt.
12 Lt.
sonography. In 1991 McClure et al again reported on the use
13t Bilat. of gray scale scrotal sonography in the evaluation of subfertile
14*· t Bilat. men. 9 They compared the results of surgical correction of
15 Bilat. Lt. clinical varicoceles (those detected by physical examination)
* Abnormal sperm motility. versus correction of subclinical varicoceles and noted that both
t Abnormal sperm concentration. groups of patients benefited from varicocele repair, with the
subclinical varicocele group realizing a slightly greater improve-
with retrograde venous flow on color Doppler evaluation were ment in semen quality than the patients with clinically identi-
not found to have a varicocele by either physical examination fiable lesions.
or gray scale sonography. These results are depicted in the Not all investigators concur, however, regarding what gray
table. scale sonographic findings indicate a subclinical varicocele. In
Of the 3 cases of a varicocele detected by all 3 techniques 2 clinical series in 1986 and 1991, McClure et al used venous
(physical examination, gray scale sonography and color Doppler dimensions and the number of identifiable veins as the primary
ultrasound) 1 was grade 3, 1 grade 2 and 1 grade 1 at physical criteria. 8 ' 9 Patients with more than 3 veins, at least 1 of which
examination. The number of subjects with varicoceles was was 3 to 5 mm. in diameter, were considered to have subclinical
small. It is not possible, therefore, to comment on the effec- varicoceles. They observed that veins larger than 5 mm. in
tiveness of each technique in detecting small versus large diameter were always palpable on physical examination and
varicoceles. would be deemed clinical varicoceles. 9 In 1987 Gonda et al
Among the subjects with a varicocele on physical examina- found that gray scale sonography compared favorably with
tion 3 (60%) had abnormal semen quality, compared to 2 (33%) radionuclide scanning in the diagnosis of varicocele. 14 They
of those diagnosed by gray scale ultrasound and 4 (33%) who considered the presence of gonadal veins greater than 2 mm. in
had retrograde venous flow on color Doppler sonography. Of diameter and increasing in size with Valsalva's maneuver to be
the 7 subjects who had previously fathered children 5 had no diagnostic of varicocele. In the same year Orda et al also found
evidence of a varicocele and 2 had reversed flow at color Doppler gray scale sonography to be clinically relevant in the evaluation
evaluation only. Most of the subjects had not attempted to of suspected varicoceles but considered the presence of 1 or
father children, so semen analysis was used as the primary more veins that increased in diameter by 1 mm. or greater with
outcome variable. Valsalva's maneuver to be diagnostic of varicocele. 15 In 1991
Neither gray scale sonography, color Doppler sonography nor Demas et al reported criteria for gray scale sonographic diag-
physical examination demonstrated a significant correlation nosis of varicoceles, designating a positive scan as showing 2
with the results of semen analysis by Fisher's exact test and or more veins, 1 of which had a diameter greater than 3 mm.
chi-square analysis. The results of physical examination ap- and increased in size with standing or Valsalva's maneuver. 16
proached statistical significance (Fisher's exact test p = 0.07, As sonographic hardware and software have become more
chi-square p = 0.04), although the semen analysis was abnormal refined, color flow Doppler sonography has found increasing
in 17% of the patients with a normal physical examination (5 application in the evaluation of a variety of disorders. In the
of 29) and normal in 40% of those with an abnormal physical evaluation of varicoceles information obtained by color Doppler
examination (2 of demonstrating low positive and negative sonography may have more physiological significance than that
predictive values. gathered with gray scale sonography, since color Doppler eval-
uation documents actual retrograde venous flow rather than
DISCUSSION venous dilatation. Thus, patients with abnormal flow but nor-
Varicocele is relatively common in the general male popula- mal venous size can be identified, As previously mentioned,
tion. In a collected series, including 9,129 men with no known Petros et al reported their experience with the use of color flow
fertility deficits, Lipshultz and Jarow reported the incidence of sonography in the evaluation of varicoceles in subfertile men. 10
varicocele identified by physical examination to range from 8 They considered the finding of retrograde flow within the
to 22.9% (mean 13.4%). 12 The incidence of varicocele is sub- pampiniform plexus, detected by color Doppler sonography, to
stantially higher, however, in the subfertile population. be diagnostic of a varicocele regardless of the dimensions of the
Lipshultz and Jarow reported that a mean of 37% of subfertile veins involved. The finding of clinical varicocele in 15% of our
men had a varicocele in a collected series of 2,121 patients study population is similar to the results of the collected series
evaluated at infertility clinics. reported by Lipshultz et al. 12 The finding ofvaricoceles in 18%
While the pathophysiology of varicocele remains a topic of of the study population by gray scale sonography is somewhat
research, varicoceles are generally believed to result from in- lower than the incidence reported by McClure et al. 8 This fact
competent valves within the gonadal vein. 13 This valvular in- may be due partly to the relatively small number of subjects
competence allows for retrograde venous flow, which is accen- included in the studies involved.
tuated with standing and performance of Valsalva's maneuver. When evaluated by color Doppler sonography, 35% of our
Venography is the most precise method of detecting potential subjects had retrograde flow within the gonadal veins consistent
retrograde flow within the gonadal vein. This procedure is with varicocele. Of the 26 subjects with normal semen quality
1538 INCIDENCE OF VARICOCELES IN GENERAL POPULATION

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