Management of Male Infertility: Roles of Contact

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Article Right varicocele and hypoxia, crucial factors in male infertility: fluid mechanics analysis of the impaired testicular drainage system

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97 Rubem Pochaczevsky1 Won J. Lee1 Errol Mallett2 Received September 12, 1985; accepted after revision January 30, 1986. 1 Department of Radiology, Department of Surgery, Long Island Jewish Medical Center, New Hyde Park, NY 1 1042. Address reprint requests to R. Pochaczevsky. 2 (ology Division, Department of Surgery. Long Island Jewish Medical Center, New Hyde Park, NY 11042. AJR 147:97-102, July 1986 0361-803x/86/1471-0097 C American Roentgen Ray Society Management of Male Infertility: Roles of Contact Thermography, Spermatic Venography, and Embolization The leading cause of male infertility is the presence of varicocele. Recently, selective spermatic vein embolization during spermatic venography has afforded a simple, nonoperative treatment. In this study, liquid crystal contact thermography was employed before spermatic venography and after embolization or surgery. Pretreatment theretographic results were in agreement with venography in 15 of 17 cases as 13 were considered positive and two negative by both methods. Thermography further served to document objectively the immediate physiologic effectiveness of either therapy in controlling spermatic vein reflux into the pampiniform plexus. It therefore provides a noninvasive means of evaluating treatment success or recurrence at an early stage. Preliminary thermographic evidence indicates that embolization is a highly effective treatment of reflux. Thermography can also function as a useful, noninvasive screening technique to aid in selecting patients for spermatic venography and embolization therapy. As early as 1956 Hanley [1 J demonstrated the association of scrotal temperature elevation due to varicocele, which is the most common cause of male infertility. According to Zorgniotti [2] spermatic vein reflux into the pampiniform plexus is the probable cause of vancocele. This reflux, with its associated intrascrotal elevated temperature, has been singled out as one of the causes of poor semen. A varicocele could also cause sterility purely on the bases of stasis of the venous circulation and associated hypoxia. Another theory postulates that metabolites from the renal vein, which reflux via the spermatic vein into the testicular pampiniform plexus, may interfere with spermatogenesis. In an earlier study Zorgniotti and MacLeod [3] also observed disturbed temperature regulation over the left hemiscrotum in many oligospermic patients without palpable varicocele. Comhaire et al. [4] analyzed these data and suggested that the temperature disturbance in these cases was caused by clinically undetectable varicocele and spermatic vein reflux. Thermography is therefore potentially useful in detecting hyperthermia during screening for such subclinical varicoceles. The frequency of varicocele in sterile men was as high as 39% in a series of 1294 patients reported by Dubin and Amelar [5] and as high as 37% among 200 patients studied by Comhaire et al. [4]. Conversely, the frequency of varicocele in the normal population has been reported to be as low as 4.4% [6]. The presence of varicocele and spermatic vein reflux, including the subclinical variety, can be demonstrated by selective spermatic venography [2, 4, 6, 7]. Recently, spermatic vein coil occlusion, performed at the time of venography, has been developed as an alternative to surgical ligation of vancoceles [8, 9]. This paper reports our results in the correlation of thermography with spermatic venography embolization therapy and surgery. It emphasizes the ability of thermography to confirm the presence of suspected varicoceles or to detect them when they are not clinically apparent.

98 POCHACZEVSKY ET AL. AJR:147, July 1986 Materials and Methods Seventeen infertile men with sperm abnormalities were evaluated by selective spermatic venography. All patients had oligospermia as well as other semen abnormalities. Liquid crystal contact color thermography using Flexi-Therm equipment(flexi-therm, Inc., Westbury, NY) was performed before venography, which was often done the same day. The liquid crystals used for clinical thermography are cholesterol derivatives, which selectively reflect polarized light in a narrow region of wavelengths. They have strong molecular rotatory powers as well as specific color-temperature responses. The latter may be accurately calibrated and used for clinical color thermography. When embedded in elastomeric Flexi-Therm sheets, the liquid crystals can be applied to any body contour, and the regional surface temperature changes are instantaneously and permanently recorded by photographic means. Details of the thermographic technique have been previously described 110]. The examination is performed in the erect position with the patient performing a Valsalva maneuver. The area of the thermogram should simultaneously include the anterior aspect of the scrotum as well as the anterior thighs (Fig. 1 ). A thermal stress maneuver to accentuate asymmetry is performed in most patients. It consists of cooling both sides of the scrotum simultaneously with an electric fan and immediately repeating the study in order to accentuate an existing thermal asymmetry or discrepancy. Embolization therapy with occluding coils was performed during selective spermatic vein catheterization (Fig. 2) if reflux into the pampiniform testicular plexus was observed. Spermatic venography was performed by placing a 9-French vascular sheath into the right internal jugular vein, superior vena cava, inferior vena cava, and left renal vein and threading a nontapered 7.3-French polyethylene catheter 65 cm in length into the left spermatic vein. The right spermatic vein was also routinely studied via the inferior vena cava in each case. A venogram obtained by injecting 10-1 5 ml of radiopaque contrast material was used to define spermatic vein anatomy and to determine the feasibility and optimal catheter position for embolization. Embolization was accomplished by using an occluding spring coil (Cook Inc., Bloomington. IN) (Fig. 2). The major advantages of coil embolization are its low cost ($1 0/coil), safety, and ease of manipulation. Coil embolization, however, should not be attempted in the presence of inordinately large collateral veins that drain directly into the iliac veins (Fig. 3) so as to minimize the risk of systemic embolization or dislodging of coils. Reflux was noted in 13 cases. Embolization was deemed safe since large collateral veins were not present, and it was technically possible to perform embolization therapy in nine of the 13 cases. High spermatic vein ligation above the pampiniform plexus near the deep inguinal ring was performed in the four cases where reflux was demonstrated but embolization was not possible for technical reasons (Fig. 3). In four cases venography did not demonstrate reflux and embolization was not carried out. Two additional patients were operated on despite normal venography when the surgeon suspected reflux on a clinical basis. Thermograms were repeated in six patients after embolization (Fig. 2) and in six patients after surgery (Figs. 4 and 5). Criteria for Interpretation L Fig. 1 -Normal thermographic examination of scrotum. Both sides of scrotum have same temperature (straight solid arrows). Normal scrotum may be same temperature as, or as in this case, slightly cooler (darker brown) than the anterior thighs (curved arrows). Penis (open arrow) is warmer (green. blue). A normal thermogram displays symmetric heat emission patterns on both sides of the scrotum (Fig. 1 ). The scrotum should have the same temperature or be cooler than the anterior thighs and the penis. A temperature differential of 0.6#{176}Cor more, encompassing at least 25% of the area of one hemiscrotum, is considered suspicious of varicocele. A temperature increase of 1 #{176}C or more is considered to definitely represent a varicocele, unless there is another pathologic process responsible for the asymmetric heat emission (Figs. 2, 3, 5, and 6). This conforms with thermographic standards of abnormality in other regions of the body [111 and with reports in the literature indicating abnormal thermal asymmetry in varicoceles ranging from 0.6#{176} to 1 #{176}C [4, 6, 12, 1 3]. A hyperthermic area can be located anywhere in the scrotum, including its upper portion (Fig. 6), and need not correspond in location to any palpable enlarged vein [5]. Bilateral varicoceles can be suspected if the entire scrotum is warmer than the anterior thighs (Fig. 7). Results A normal spermatic venogram without reflux was noted in four of 1 7 cases. Thermography was also negative in two of these cases (Fig. 1). However, in the remaining two cases, thermography was interpreted as compatible with a left varicocele, since there were no other clinically appreciated pathologic processes that could account for the hemiscrotal temperature increase. Clinical examination confirmed the presence of a varicocele in these two patients, who then underwent high surgical ligation of the spermatic vein. Thermography was in agreement in all 1 3 patients in whom the spermatic venograrn showed reflux of contrast material into the testicular pampiniform plexus (Figs. 2, 3, and 6). Only one patient had reflux confirmed to the right side. The thermogram simultaneously showed a right varicocele in this instance. In five of the 1 3 cases in which reflux was demonstrated by both venography and thermography, the diagnosis of varicocele was not apparent by physical examination. They were, therefore, indicative of subclinical varicoceles. Postembolization thermography was repeated in six patients. It showed conversion to a symmetric and normal

AJR:147, July 1986 MALE INFERTILITY 99 Fig. 2-34-year-old infertile man. A, Scrotal thermogram shows increased heat emission on left (arrow) compatible with varicocele. B, Left retrograde spermatic venogram confirmed presence of a left varicocele (arrow). c, This was followed by occlusive coil embolization (arrow). D. Repeat thermogram 5 days later shows complete symmetry of both sides of scrotum (straight arrows). When thermograms return to normal, successful embolization therapy is confirmed. thermogram in all cases, documenting good physiologic response to treatment (Fig. 2). Two of the six patients became fertile. Another two remained infertile for 6 months and 2 years, respectively, after embolization; in one of these patients, only a small increase in sperm count (from 1 5 to 20 million) was noted. However, the other patient had a significant increase in sperm count, from 8.6 to 55 million, with an improved motility pattern (Fig. 2). The remaining two patients, aged 1 6 and 17 years, were embolized because of painful varicoceles. No fertility evaluation was undertaken. They both improved symptomatically. Postsurgical thermograms were performed in six patients (Figs. 4 and 5). In one patient, thermography 1 month after high surgical ligation of the left spermatic vein revealed decreased heat emission from the operated left side, so that a right varicocele was simulated. Nevertheless, a normal right scrotum was correctly identified since its heat emission pat- tern was similar to that of the anterior thighs (Fig. 4). His low sperm count persisted. Thermography in two patients 3 days and 9 months, respectively, after surgery documented normalization of the preoperative thermal asymmetry. Sperm counts 9 months and 1 year after surgery, however, showed only marginal improvement in these two patients. Counts rose from 6 to 12 million in one patient and from 1 5 to 1 8 million in the other. In two other patients, thermographic evidence of recurrence of the varicocele was noted within 1 month (Fig. 5) and within 2 weeks after surgery. The first patient showed a minimal rise in sperm count from 1 2 to 1 5 million, 8 months after surgery. The second patient fathered his first child 6 months after having undergone successful embolization. Another patient (1 7 years old) showed normalization of his thermogram after surgery. No fertility studies were performed because surgery was performed for a painful varicocele. Pain was entirely relieved postoperatively.

100 POCHACZEVSKY ET AL. AJR:147, July 1986 Fig. 3-17-year-old with painful left varicocele. A, Thermogram of scrotum shows increased heat emission from entire left hemiscrotum (solid arrow), indicative of left varicocele. Penis is denoted by open arrow. B, Selective spermatic venogram shows considerable left spermatic vein reflux (straight arrow) and large collateral vein (curved arrow). c, Radiograph taken seconds later shows large collateral vein (straight arrow) draining directly into left iliac vein (curved arrow) and inferior vena cava. In view of marked collateral circulation, embolization was deemed unsafe. Patient s pain subsided after surgery. Discussion Thermography showed excellent correlation with selective spermatic venography in demonstrating the presence or absence of varicocele in 15 of our 17 patients evaluated for infertility (Figs. 2, 3, and 6). In the only two patients in whom the results of thermography and venography differed, yenography was falsely negative, since a varicocele was noted clinically. Results indicate that thermography can be used as a sim-

AJR:147, July 1986 MALE INFERTILITY 101 F.a.. =, -.,. %, =- -,,,, decreased heat emission lam operated side. Apparent hyperthermia (lighter brown and yellow) from right hemiscrotum (straight solid arrow) compared with left. However, heat emission pattern on right is identical to anterior thighs (curved arrows). Penis is indicated by open arrow. Physical examination was negative. pie, noninvasive screening test for selective spermatic vein venography. The latter is a highly reliable but invasive radiologic examination. Thermography objectively documented the effectiveness of embolization therapy in controlling reflux into the testicular pampiniform plexus in six cases in which a repeat thermogram was obtained (Fig. 2). It therefore lends support to the role of embolization in the treatment of male Fig. 5.-Thermography 3 months after left spermatic vein ligation for varicocele in 28-year-old infertile man. Note increased heat emission (arrow) from left hemiscrotum compared with right, indicating presence of recurrent left varicocele. I. Fig. 6.-Scrotal thermogram of 26-year-old infertile man shows a small hyperthermic area in upper left scrotum diagnostic of small varicocele (green, arrow). Physical examination was negative. Selective spermatic venography demonstrated minor degree of left spermatic vein reflux into testicular pampiniform plexus. Surgical ligation was performed. Patient s low sperm counts became normal within 3 months and he fathered his first child 6 months after surgery. infertility. Although these preliminary results of spermatic vein embolization therapy are highly encouraging, it is still too early to assess its ultimate efficacy. Conversely, surgical ligation of the spermatic vein has proved to be effective in infertile men with sperm abnormalities and clinical evidence of varicocele [4-6, 1 2-1 5]. Among the 504 infertile men with semen abnormalities and varicoceles who underwent surgical ligation reported by Dubin and Amelar [5], the semen quality improved in 71 % within 1 year and 55% became fertile. However, if a varicocele is not clinically evident, the beneficial results achieved by surgery decrease considerably. This is illustrated by the report by Fogh-Andersen et al. [1 6] that only seven (32%) of 22 sterile men with semen abnormalities, but without clinically apparent varicocele, became fertile after surgery. In their control group of 44 men, 5% became fertile without surgery. The value of thermography in selecting patients for treatment is particularly important when the presence of varicoceles cannot be definitively diagnosed by physical examination. This was shown in the five patients in whom a varicocele was detected solely by thermography and subsequently proved by venography. The ability of thermography to detect these subclinical varicoceles was also shown by Comhaire et al. [4]. They reported that 1 9 infertile patients without clinical evidence of varicocele had positive thermograms. Subse-

102 POCHACZEVSKY ET AL. AJR:147, July 1986 Fig. 7.-Scrotal thermogram shows symmetric hyperthermia of the scrotum (green. straight arrows) compared with anterior thighs (curved arrows) indicative of bilateral varicoceles. quent selective spermatic venography demonstrated reflux into the testicular pampiniform plexus in 1 6 cases. On the other hand, venography showed reflux in only one of five patients with normal thermograms. In addition, Comhaire et al. [4] showed that the thermogram had high specificity for the detection of varicoceles since it was normal in all 23 controls without varicoceles. Similar results were obtained by Lewis and Harrison [13], who found an average hemiscrotal asymmetry of slightly more than 1 #{176}C in 24 patients with infertility and semen abnormalities who were considered to have subclinical varicocele. He also found that 43 patients with clinical varicocele had an average asymmetry of 0.8#{176}C, while normal controls were largely symmetric with most displaying differences of only 0.2#{176} to 0.3#{176}C. Role of Thermography in the Posttreatment Period Improvement of semen count may not become apparent until 6 months or more after surgery for varicocele. However, thermography is useful in predicting treatment success because reversion to a normal thermal pattern may be evident several days after treatment (Figs. 2, 4, and 5). In the study by Lewis and Harrison [13], four of the six patients who had high spermatic vein ligations for varicoceles showed complete thermographic symmetry after surgery. Two of these men became fertile. The mean asymmetry of the entire group before surgery was 0.87#{176}C.One patient showed a 0.9#{176}Casymmetry and had evidence of persistent left spermatic vein reflux. One patient did not have postoperative thermography. Of the 45 patients reported by Monteyne and Comhaire [1 5], 1 1 had persistent hyperthermia on the operated side. Ten of these cases had evidence of venous reflux on the retrograde venogram. Of the remaining 34 patients, 27 had complete symmetry and seven had a lower temperature or a desirable decrease in their hyperthermia on the operated side. In our series, thermographic changes observed after embolization (Fig. 2) or surgical ligation (Figs. 4 and 5) were used as objective guides in the evaluation of treatment results. Comparison of Thermography with Other Diagnostic Methods In addition to spermatic venography, contact sonography, Doppler sonography, and scintigraphy can be used in the evaluation of varicoceles. Sonography can easily image dilated scrotal veins [17]. However, thermography provides information regarding the effect of a varicocele on fertility [2] whereas sonography simply demonstrates its presence. Doppler sonography has also been reported to be an accurate diagnostic test for varicocele [6], while scintigraphy has been reported to have a low accuracy rate in diagnosing varicocele [1 8]. Neither test was performed in this study. REFERENCES 1. Hanley HC. Surgical correction of errors of testicular temperature regulation. Proc. 2nd World Congr Fertility and Sterility. Naples 1956:p. 953 2. Zorgniotti AW. Elevated intrascrotal temperature. I. A hypothesis for poor semen in infertile men. Bull NY Acad Med 1982;58: 535-544 3. Zorgniotti AW, MacLeod J. Studies in temperature, human semen quality, and varicocele. Fertll Steril 1973;24: 854-863 4. Comhaire F, Monteyne A, Kunnen M. The value of scrotal thermography as compared with selective retrograde venography of the spermatic vein for the diagnosis of subclinical varicocele. Ferti! Steri! 1976;27(6): 694-697 5. Dubin L, Amelar RD. Varicocelectomy as therapy in male infertility: study of 504 cases. Fertil Steril 1975;26:21 7-220 6. Kormano M, Kahanpaa K, Svinhufvud U, Tahti E. Thermography of varicocele. Fertil Steril 1970;21 :558-564 7. Pararno PG, Guirado FR, Paramo PS Jr, Silmi A, Uson AC. Valor e indicaciones de Ia ultrasonografia Doppler en Ia investigacion diagnostica del varicocele. Acta Urol Esp 1981;5: 111-118 8. White RI Jr, Kaufman SL, Barth KH, Kadie S, Smyth JW, Walsh PC. Occlusion of varicoceles with detachable balloons. Radiology 1981;139:327-334 9. Berkman WA, Price RB, Wheatley JK, Fajman WA, Sones PJ, Casarella WJ. Varicoceles: a coaxial coil occlusion system. Radiology 1984;151 :73-77 10. Pochaczevsky R, Pillari G, Feldman F. Liquid crystal contact thermography of deep venous thrombosis. AJR 1982;138:717-723 11. Feldman F, Nickoloff EL. Normal thermographic standards for the cervical spine and upper extremities. Skeletal Radio! 1984;1 2: 235-249 12. Harrison AG. Male infertility. Proc R Soc Med 1966;59:763-765 13. Lewis RW, Harrison AM. Contact scrotal thermography. II. Use in the infertile male. Fertil Steril 1980;34:259-263 14. Comhaire FH. Radiological exploration and thermographic data of varicocele. Acta Eur Fertil 1977;8(4): 273-281 1 5. Monteyne A, Comhaire F. The thermographic characteristics of varicocele: an analysis of 65 positive registrations. Br J Urol 1978:50:118-170 16. Fogh-Andersen P, Nielsen NC, Rebbe H, Stakemann G. The effect on fertility of ligation of the left spermatic vein in men without clinical signs of varicocele. Acta Obstet Gynecol Scand 1975:54 :29-32 17. Aifkin MD, Foy PM, Kurtz AB, Pasto ME, Goldberg BB. The role of diagnostic ultrasonography in varicocele evaluation. J Ultrasound Med 1983;2:271-275 18. Cornhaire F, Vandeweghe M, Simons M. Comparison between thermography and venous scintigraphy of the scrotum in the diagnosis of varicocele. lnt J Androl 1981 4: 663-668