Phlebography, first introduced in 1966 by Ahleberg (9),is generally accepted as the “goldstandard―for the depiction of varicocele (10—12).It is nevertheless invasive,uncomfortable, carries some risks and is not physiologic(13). For these reasons, other diagnostic approaches, suchas thermography (14), scintigraphy (15,16), ultrasound(17,18) and echo-Doppler (19), have been proposed, withthe aim of finding an imaging modality as sensitive asphiebography, but without its drawbacks.

By means of various imaging techniques, it has beenpossible to distinguish between a palpable enlargement ofthe pampiniform plexus, defined as clinical varicocele,which may be staged as Grades 1, 2, and 3 by the classification of Dublin and Amelar (20), and sub-clinical vancocele defined as reflux through the internal spermaticvein, without any palpable distension of the pampiniformplexus (21). Many of the papers published on the topicdeal with the associated alterations ofspermatogenesis andconsequently highlight the ability to detect subclinicalvaricocele, since this is considered by some to be as importantas clinical varicocele in decreasing fertility(13,22—25).

The purpose ofthis study was not to evaluate the abilityof the various imaging techniques to distinguish clinicalfrom subclinical varicocele as defined above, because wedid not study patients presenting with infertility. Ratherwe examined the ability of radionucide studies, thermography and ultrasound, to objectively confirm the presenceof varicocele which was clinically diagnosed or suspectedon the basis ofpatient discomfort or physical examination.We also compared the grading of these techniques withthat of phlebography. In the majority of our patients, theresults of semen analysis (sperm counts, motility andmorphology) were available and were correlated with thethree phlebographicgrades of vaicocele.

MATERIALS AND METHODS

From 1987 to 1989 we studied 263 patients in whom avaricocelehad been diagnosed(185 cases)or suspected(78cases)on the basis of patient complaints of swelling, discomfort orphysical examination.

We did not study patients presentingwith infertilityand ab

VaIICOCeIe,a varicosity of the pampiniform plexus, usually onthe left side, is a common urologic problem. It may be associated with symptoms of local discomfort or abnormal sparmatogenesis. Internal spermatic vein phlebography is theTMgoldstandard―investigative technique, but it is invasive.Noninvasivestudiesinclude:labeledblood-poolscintigraphy,thermographyandultrasound.Twohundredsixty-threepatients were investigatedwith variouscombinationsof thesemOdalitieS.The degree of abnormality for each modality wasgradedsemiquantitativelyandtheresultscompared.Inaddition, the results of semen analysis were correlated to imagingresults. Ninety-six patients were investigated with all fourtests (santigraphy, thermography, ultrasound and phlebography). The correlation of positive phlebography to positivescintigraphy was 98%, to thermography 100% and to ultrasound98%.Theconcordance(gradefor grade)was 71% forscintigraphy, 68% for thermography and 62% for ultrasound.Therewasnoobviouscorrelationbetweenabnormalitiesofsemenanalysisandgradingof vancocele.We concludethatthe diagnostic accuracy and grading of severity by noninvasive techniques(includingscintigraphy)comparevery favorablywiththatof phlebography.Moreover,scintigraphyallowsthe noninvasive evaluation of reflux through the internal sparmatic vein, which may be useful in planning therapy.

J NucIMed 1991;32:2092—2097

aricocele is a varicosity of the veins of the pampiniform plexus, probablydue, as suggestedby Ivanissevich in1981, to a reflux of blood via the internal spermatic vein(ISV)(1). This can resultfrom an absence or incompetenceof the venous valves, collateral by pass vessels and/or anincreased pressure gradient between the inferior vena cavaand the left renal vein (2,3).

In 80%—97%of cases, the varicocele involves only theleft side; it may be bilateral in up to 20%, although theright sided varicosity is usually smaller (4—7).A unilateralright sided varicocele is very uncommon (8).

Received Sept. 17. 1990; revIsion accepted May 7, 1991.For reprints contact: Onello Geath, MD. Istituto di Medians Nucleare,

OspedaleCMIe. 33100 Wine. Italy.

2092 TheJournalof NuclearMedicine•Vol.32•No.11 •November1991

A Comparison of Scintigraphy, Thermography,Ultrasound and Phiebography in Grading ofClinical VaricoceleOnelio Geatti, Daniele Gasparini, and Brahm Shapiro

Istituto di Medicina Nucleare and Instiluto di Radiologia II, Ospedale Civile, Udine, Italy and Division ofNuclear Medicine,Department oflniernal Medicine University ofMichigan Medical Center, Ann Arbor, Michigan

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normalities of semen analysis unless they also had a clinicallysuspected or verified varicocele. The mean age was 22.8 yr (s.d.7.2 yr). A large fraction of our patients (over 80%) came fromthe armyand this may explain the narrowage s.d. Militaryservicestartingat 19yr is mandatory in Italy. Regulationsmay exemptinductees from service if they suffer from significant varicocele.Thus, those seekingto avoid servicemay complain in the absenceof varicoceleand thoseseekinga military careermay find vancocele a barrier, unless the condition is effectively treated. Underthesecircumstances,there isa needforaccurate,noninvasiveandobjective techniques for the documentation and gradingof vancocele.

Of the 263 patients studied with various combinations oftechniques (Table 1),96 were studied with phiebography,scintigraphy, thermography and ultrasound. Semen analysis was ohtamed in 146 patients.

ScintigraphyScintigraphic evaluation was performed with the patient in the

uprightposition,the legssomewhatapart, the penis taped to themidline of the anteriorabdominal wall and the scrotum locatedin the lower third of the field of view. The patient's red bloodcells were in-vivo labeled by injecting 0.15 gig/kg ofstannous ionsin the form of pyrophosphate 20 mm before the intravenousadministration of 370 MBq [@mTc]pertechentate.Imagingwasperformedusinga small fieldof viewgamma camera (S.E.L.O.,Italy)equippedwith a parallel-hole,low-energycollimatorand azoom factor of 1.4. Sixty 2-sec images were acquired in a 64 x64 byte matrix on an online minicomputer (Maps 2000, LinkSystem, UK) startingwith the rapid bolus injection (less than 1cc) of 370 MBq (10 mCi) [99mTc]pe@.@hnetate via a forearmvein. The 2-sec framesthus acquiredwere summed as sequential8-sec and 30-sec frames for interpretation and hardcopy records.

Subsequentlya 300-secimage,usuallywith more than 500Kcounts, was obtainedand this was consideredto depict the bloodpool. To improve contrast and facilitate interpretation, a threshold of up to 40%-50%was used when needed.

TABLE IPatientsStudiedby VariousModalities

Leftinternalsperrnaticveinphiebography,thermography,ultrasound

Leftinternalspermaticveinphiebography,rightintemal spermatic vein phlebography, scintigraphy,thermography,ultrasound

Leftntemalspermaticveinphlebography,scintigr@ iy, thermography

Leftntemalspermaticveinphiebography,scintigra @y,ultrasound

Leftnternalspermaticveinphiebography,therif yaphy, ultrasound

Left nternalspermaticveinphiebography,scintigrI @y

Left ntemalspermaticveinphiebography,therrr3raphy

Leftinternalspermaticveinphlebography,ultrasound

Leftinternalspermaticveinphlebography(only)Scintigraphy,thermographyScintigraphy,ultrasound

Total

Occasionally vasovagal symptoms occurred, but these rarelyinterrupted the study. When they did, it was during blood-poolimaging and a sufficient number of counts was always acquired

so that a final interpretation was possible (15).

ThermographyThis was performed with the patient in the upright position

after an adaptation period (15-20 mm) to room temperature,which was kept constant at 20—22°C.The scrotum was thermallyisolated from the body and the penis taped to the midline of theanterior abdominal wall. Anterior and oblique viewswere ohtamed using an AGA Thermovisionunit, number 680, with atemperaturediscrimination of0.5°C.Quality control was maintamed using a thermal marker kept at a constant 31°Cforstandardization and control of instrument stability (14,21).

UftraeoundUltrasound was performed with the patient in the supine

position at rest and during a Valsalvamaneuver. The scrotumwas scanned in the longitudinal and transverse planes (Fig. 1)usinga Hitach 7.5 MHz linearprobewith a spatialdiscriminationability below 1 mm (17,18,21).

Selective Spermatic Vein PhlebographyThis was performed by means of a selective catheter usually

inserted through the right femoral vein and injection of 10—20ml contrast medium (2-3 mI/see) with the patient semiupnight(30°—50°)usinga Zeitler type catheterfor the left (Fig. 2) and aside-winder catheter for the right internal spermatic vein (9—12).

Semen AnalysesThese were obtained according to standard techniques (26):

sperm number was quantified as million/mi, while morphology

and motility (after2 hr)were expressedas percentageof structurally normal cells and spermatozoa having “activeforward motility,―respectively.

82

14

54

8

13

4

11

3

FIGURE1. Scrotalultrasound(axialviews).(A)Duringquiet7 respiration.Normalright testis (largearrow). Left testis with

66 slightlydilatedveins in the pampiniformplexusdemonstrated as1 smallanechoicfoci with some reinforcementof the posterior

walls (small arrows). (B) During Valsalvamaneuver.Striking in263 crease in diameter of dilated vein to 5 mm (Grade 3)(small arrow).

2093Scintigraphic Grading of ClinicalVariCOcele•Geath et al

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CRITERIAFOR INTERPRETATIONOF RESULTS

Results obtained from the different imaging modalitieswere classified on a scale from zero to three, according tothe following criteria:

Blood-Pool Sclntlgraphy

0 = normal study (Fig. 3A).1 = mild uptake (just above background) (Fig. 3B).2 = moderate uptake (less than major normal vascu

lar structures) (Fig. 3C).3 = intenseuptake(comparedto major normalvas

cular structures) in a half or entire scrotum andalong the internal spermatic vein (Fig. 3D).

The images taken duringthe flow phase were consideredto be an expression ofthe degree ofvenous reflux, and theblood-pool scan was felt to reflect the vanicocele volume(27). Varicocele grading was performed primarily on theblood pool images which are more comparable with ultrasound and thermography,as these depict only the vanicocele volume and not the blood flow. In addition, weexamined the flow phase, to verify whether significantreflux of blood occurred through the internal spermaticvein and whether the degree of reflux was related to thevolume ofthe varicocele. To do this, we found it necessaryto add four frames togethen to get a series of 8-sec images(Fig. 4). For better visual presentation of the studies, wealso presented nuclear angiograms as four 30-sec addedimages starting from the time ofinjection (Fig. 5).

BloodFlowSclntlgraphy

0 = no reflux.1 = minimal reflux (just above background).2 = moderate reflux (less than intensity of simulta

neously visualized vascular structures).3 = marked reflux (equal to intensity of simultane

ously visualized vascular structures).

Thermography

0 = normal study (3 1°C)1 = 32°C2=33°C3 = 34°Cor greater

Uftrasound

0 = no change in pampimform plexus diameter, considered normal up to 2 mm.

1 = very slight dilatation, up to 3 mm.2 = moderatedilatation, up to between3 and 5 mm.3 = major dilatation, more than 5 mm.

Phlebography

0 = no reflux, continent valves.1 = reflux in the ISV with a diameter less than 5 mm

FIGURE 2. Left ISV phiebographydemonstratinga moderate(Grade2) van

and opacification of a slightly enlarged pampiniform plexus.

2 = reflux in the ISV of a diameter between 0.5 and1 cm and an evident varicocele.

3 = reflux in the ISV with a diameter greater than 1cm and a wide varicocele.

SemenAnalysis

0 = more than 60 million sperm/ml, motility andnormal cell morphology greaterthan 80%.

1 = between 25 and 60 million sperm/mi and/ormotility and normal cell morphology between50% and 80%.

FIGURE3. Examplesof blood-poolscintigraphydemonstrating: (A) Grade 0 (normal study), (B) Grade 1 (minimal uptake), (C)Grade 2 (moderateuptake),and (D)Grade 3 (intenseuptake).

2094 TheJournalof NuclearMedicine•Vol.32•No.11 •November1991

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:‘@ I

, ‘@

.@.‘,@@@ /‘

@@@ I

: “@@ f@@ 4@•t@

@ 0@

Phlebography321(grading)(50patients)(35 patients)(9 patients)

* Concordance was grade for grade between modalities. Overall

agreementfor all patientswas 71% for scintigraphy,68% for thermography and 62% for ultrasound.

and 6%, respectively. In no case did thermography orultrasound overestimate by two grades.

A one grade underestimation occurred in 11%, 12%,and 27% with scintigraphy, thermography, and ultrasound, respectively. An underestimation by two gradeswas obtained in 1%by scintigraphy and in 4% by ultrasound. In no case was there an underestimation of twogrades by thermography (Table 3).

For a majority ofthe 94 patients with positive phiebography, the scintigraphic flow-phase demonstrated reflux ofthe same grade as varicocele volume (86 of 94, 91%). Inthe remaining eight cases there was an underestimation oftwo grades in one case and of one grade in another and anoverestimation of one grade in six cases. There was nopatient with a left-sided varicocele, without at least a mildincrease in flow through the left ISV demonstrable by flowphase scintigraphy.

In 8 of the 14 patients who had right-sided ISV phlebography, this was normal, confirming the findings byscintigraphy, thermography and ultrasound. In the othersix, phiebographywas positive as were scintigraphy, thermography and ultrasound. The disease was graded phlebographically as Grade 2 in two cases and Grade 1 in four(Scintigraphy was positive for a right varicocele in a totalof 23 patients and this was confirmed by phlebography in6, by thermography in 5, and by ultrasound in 1.)

Sixty-seven patients with only mild clinical suspicion ofvaricocele (left) had at least two negative noninvasivestudies and were not subjected to phlebography and wereconsidered not to have varicocele.

In Table 4, correlations between semen analysis and

I \

@@ :

(@f(.f.TABLE3Percentages

of Overall Concordance for Each ImagingModality Compared to Phlebography in the 94 Patients with

a PositivePhlebogramScintigraphy

ThermographyUltrasoundConcordance

71 6862+1overestimate 14 206+2overestimate 2 00—1underestimate 11 1226—2underestimate 1 04False-negative

1 0 2

TABLE 2Concordance in Grading Between Scintigraphy,Thermography, Ultrasound and Phlebography*

FIGURE4. Exampleofflowphasescintigraphy demonstratingGrade3 refluxviatheleft ISV.(Series of 8-sec frames, addedfrom2 secperframeacquisition). __________________________________

2 = between 5 and 25 million sperm/ml and/or motility and normal cell morphology between 30%and 50%.

3 = up to 5 million sperm/mi and/or motility andnormal cell morphology up to 30% (13).

RESULTS

Among the 96 patients studied by scintigraphy, thermography and ultrasound who also had phlebography,each imaging modality was positive in the 85 patients witha clinically diagnosed varicocele (Grades 1—3for phlebography). In the 11 patients with a clinically suspected varicocele, 9 had a positive phlebogram (Grades 1 or 2) andwere also positive by scintigraphy, thermography and ultrasound in 8, 9 and 7 patients, respectively.

The three false-negative noninvasive studies (one forscintigraphy and two for ultrasound) had Grade 1 varicoceles by phlebography. In the two patients with a clinicallysuspected varicocele and normal phlebography, a falsepositive study was obtained in one case by ultrasound andin another by both scintigraphy and thermography (allGrade1).

Table 2 presents the correlations between grading byscintigraphy, thermography, ultrasound and phiebographywith an overall agreement, grade for grade, from 62% forultrasound to 71 % for scintigraphy. The closest correlations were obtained in the highest grade ofvaricocele, witha positive correlation of 82% by scintigraphyand 80% bythermography, respectively. In looking at the discrepanciesin grading, we observed that scintigraphy overestimatedby one grade in 14% and two grades in only 2%; thermographyand ultrasound overestimated by one grade in 20%

ScintigraphyThermographyUltrasound

41 (82%)40(80%)28(56%)

23(65%)19 (54%)25(71%)

3(30%)5(56%)5(56%)

FIGURE5. Exampleof flow phasescintigraphy demonstratingGrade3 refluxviatheleft ISV(series of 30-sec frames, addedfrom 2 sec per frameacquisition).

2095Scintigraphic Grading of ClinicalVaricOcele•Geatti et al

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TABLE 4Semen Analysis Abnormalities (Grades 1-3) Related to

Phlebography Patient Groups (Grades 1—3)

Semen analysis (3) (55%)5 (49%) 17 (62%)31Semenanalysis(2) (11%)1 (26%) 9 (28%)14Semenanalysis(1) (33%)3 (26%) 9 (10%) 5

Phlebographic grading (Group 1) 9 (Group 2) 35 (Group 3)50

phlebography grading are shown. There is a similar percentage (about 60%) of the most severe degree of spermabnormality in all grades of phlebographic abnormality.

DISCUSSION

Our results with a large series of patients confirm thereliabilityof scintigraphy,thermography and ultrasoundin detecting and objectively confirming clinically diagnosed or suspected varicocele and, as such, are in keepingwith published data (14-21). Sensitivity as high as 92%and specificity of97% have been reportedfor scintigraphyversus a venographic gold standard (32). We believe thatby using these noninvasive techniques it may be possibleto identify those patients who may benefit from a thempeutic intervention. Before proceeding to phiebography,when a varicocele is suspected on clinical grounds, thenoninvasive imaging modalities may be performed as ascreening device.

Scintigraphy is able to demonstrate the blood flow refluxthrough the ISV, allowing the evaluation of filling rate (inthe “flowphase―)and varicocele volume (in the bloodpool image) (27). These closely correspond to phlebographic sizing and thus be useful for comparison aftertherapeutic interventions to verify adequacy of cure orseverityofrecurrence. Moreover, the flow phase of scintigraphy may distinguish ISV reflux from obstruction of thehypogastric or iliac vessels. The latter is a rare cause ofvaicocele but, when present, carries serious prognosticimplications.

Finally, the evaluation of reflux through the ISV maybe useful in discriminating between recurrences due tospermatic vein collaterals and flow through perirenal ordistal pelvic vessels.

Each of these noninvasive techniques yield comparableoverall results in grading vanicocele volume. We believescintigraphyto be less operator-dependent than thermography and ultrasound for both performance and interpretation. We thus believe scintigraphy to be a valid noninvasive technique to objectively document and grade theseverity of clinically diagnosed or suspected varicocele. Inthe specific patient population studied, the need for anaccurate noninvasive study yielding objective documentation ofvaricocele is ofspecial importance and may havea major impact on the lives and careersof the young meninvolved. The nature of the patient referral pattern hasresulted in a patient population that is different frompreviously studied groups in which infertility, with or

without clinical varicocele, was a major indication forstudy (2,4,12—15,19,20,22).

We confirmed a much lower incidence of a right-sidedvaricocele, which in our series never occurred without asimultaneous left side involvement (4—8).

Semen analysis revealed the absence of any obviouscorrelation between varicocele size and the severity ofseminal abnormalities. The young mean age of our patients (22 yr) could have resulted in a shorter duration ofthe disease which might explain these results. We did notstudy patients with infertilitywho had no clinical evidenceof vanicocele. The relationship of varicocele to infertilityremains somewhat controversial; nevertheless, in at leasta subset of patients there does appear to be a cause andeffect relationship that may be reversed by the treatmentof the varicocele. The mechanism of this phenomenon isalso somewhat controversial but may be related to thereflux ofcore temperatureblood into the varicocele whichraises testicular temperature above that for optimal spermatogenesis (29—31).

ACKNOWLEDGMENTS

The authors thank Ema Coy, Augusto Peressoni, MarinaRossi,ErmesStellaand SilvanaTosolinifor technicalassistance;Pierina Saria and Lina Ferro for nursing;and Ms. D. Burch forexcellentsecretarialassistance.

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2097Scintigraphic Grading of ClinicalVaricocele •Geatti et al

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1991;32:2092-2097.J Nucl Med.   Onelio Geatti, Daniele Gasparini and Brahm Shapiro  Grading of Clinical VaricoceleA Comparison of Scintigraphy, Thermography, Ultrasound and Phlebography in

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