• No results found

The Adolescent Varicocele: What’s New With an Old Problem in Young Patients?

N/A
N/A
Protected

Academic year: 2020

Share "The Adolescent Varicocele: What’s New With an Old Problem in Young Patients?"

Copied!
13
0
0

Loading.... (view fulltext now)

Full text

(1)

The Adolescent Varicocele: What’s New With an Old Problem in Young

Patients?

Steven J. Skoog, MD*; Kenneth P. Roberts, PhD‡§; Marc Goldstein, MD¶; and Jon L. Pryor, MD‡§i

ABBREVIATIONS. GnRH, gonadotropin-releasing hormone; LH, luteinizing hormone; FSH, follicle-stimulating hormone.

A

ccumulating evidence from animal and

hu-man studies has demonstrated that varicoce-les are associated with a time-dependent de-cline in testicular function.1– 4As a result, the finding of dilated scrotal veins, a varicocele, in an adolescent presents the practicing physician with a number of problems: When should one surgically intervene in the adolescent? Although infertility is not a present-ing complaint, should prophylactic varicocele repair be performed to prevent future infertility and possi-ble testosterone deficiency?

These questions can only be answered when we have a better understanding of the pathophysiology of the varicocele. The purpose of this review is to present the most current information on the adoles-cent varicocele, provide guidelines on managing this perplexing problem in the asymptomatic adolescent male, and stimulate future research about the enig-matic relationship between the varicocele and its effects on testicular growth and function.

EPIDEMIOLOGY

Approximately 15% of all adult males have a var-icocele.5One-third of all males evaluated for infertil-ity have a varicocele, demonstrating the negative impact of varicoceles on testicular function.6 How-ever, only 15% to 20% of males with a varicocele seek treatment for infertility, suggesting that most males with a varicocele are fertile or do not seek treatment. Although varicoceles have been reported in the preadolescent male, they are rare in this age group.7,8 In a survey by Oster9 (1971) of 1072 school boys in Denmark, there were no varicoceles found in 188 boys who were between the ages of 6 to 9 years. The incidence of varicoceles in the older child, (ages 10 to 25), varies between 9% to 25.8% with a weighted average of 16.3% (Table 1).9 –14This is similar to the incidence of varicoceles in the adult population and

suggests that the physiologic changes associated with puberty, such as an increase in testicular growth and, presumably, an increase in testicular blood flow, are responsible for varicocele formation in ad-olescents.

ANATOMY

The arterial blood supply to the testis comes from the testicular artery, the deferential (or vasal) artery, and the cremasteric (or external spermatic) artery. Although the testicular artery is the major source of blood for the testis, there is collateral communication between these three arteries at the level of the testis; 15,16this collateral circulation can usually supply

suf-ficient blood to the testis if the testicular artery is ligated during varicocele repair.17

As is true in most organs, the pattern of venous drainage of the testis largely follows that of the ar-terial supply. However, the venous drainage of the testis is very complex by design and, as a result, is highly variable in its details (Fig 1).18 –22As the veins of the testis emerge from the tunica albuginea they form a dense network of intercommunicating branches known as the pampiniform plexus. The pampiniform plexus begins in the scrotum and ex-tends into the spermatic cord. The arteries supplying the testis course through this plexus and the arterial blood is cooled from abdominal temperature (37°C) to testicular temperature (33°C) by counter-current heat exchange with the veins of the pampiniform plexus.

The venous drainage from the pampiniform plexus is via the testicular, pudendal, and cremas-teric veins (Fig 1). The right testicular vein joins the ascending vena cava, inferior to the right renal vein, whereas the left testicular vein joins the left renal vein. The testicular veins have a number of variable branches (Fig 1).18 –22 In addition, cross-anastomosis between the left and right testicular venous systems has been reported in some men.19,20,23 The vasal or deferential vein, associated with the vas deferens, can provide venous return from the testicle after ligation of the varicocele.

ETIOLOGY

Palpable unilateral varicoceles occur on the left side in 85% to 90% of cases.24 A palpable right vari-cocele is normally found in cases of bilateral varico-celes and rarely occurs unilaterally.24 The high pre-ponderance of left-sided varicoceles, combined with

From the *Department of Urology, Oregon Health Sciences Center; ‡De-partments of Urologic Surgery, §Neuroanatomy and Cell Biology, and

iObstetrics and Gynecology, University of Minnesota Medical School; and the ¶Department of Urology, New York Hospital-Cornell Medical Center. Received for publication Feb 7, 1996; accepted Jun 4, 1996.

(2)

the unique anatomy of the left testicular vein, is the basis for several theories explaining the etiology of a varicocele. First, it has been proposed that because the left testicular vein is longer than the right testic-ular vein, the hydrostatic pressure in the distal re-gion of the left testicular vein is unusually high. However, this anatomy is very constant and would be expected to cause varicoceles in all men if it were the only cause. Second, a lack of valves in the testic-ular vein would result in increased pressure trans-mitted to the testicular vein from the renal vein. However, autopsy studies have shown that valves are not always present in the normal testicular vein and there is not a preferential lack of valves in the left testicular vein.19,20,25–27 Third, the left renal vein, by virtue of its course anterior to the descending aorta and posterior to the superior mesenteric artery, is

predisposed to compression; this compression has been termed the nutcracker effect.28 The resulting increase in renal vein pressure is transmitted to the testicular vein, contributing to its dilatation. This is a feasible hypothesis because increasing the pressure in the left renal vein leads to varicocele formation in many experimental animals.29Although high left re-nal vein to vena cava pressure gradients have been noted in patients with varicoceles, it is not a consis-tent feature.30 –32

In summary, none of the vascular anatomical fea-tures have been proven to be the cause of a varicocele. It is likely that the etiology of the varicocele is mul-tifactorial.

PATHOPHYSIOLOGY

Experimental varicoceles in animal models, cre-ated by partial constriction of the left renal vein medial to the junction of the left testicular vein, have been used to investigate the pathophysiology of the varicocele.29,33Many features of the human condition, such as increased testicular temperature and altered blood flow, are replicated in this animal model. Re-pair of experimental varicoceles results in improved testicular function.29,34Several potential mechanisms on how the varicocele causes testicular defects have been proposed.

Hyperthermia

Clinically the varicocele is associated with ele-vated temperature of the scrotum and testes, which is detrimental to spermatogenesis.35–37 DNA poly-merase activity and the enzymes of DNA recombi-nation in germ cells are temperature-sensitive, with optimal activity at 33°C, and protein synthesis in round spermatids has been shown to be optimal at 34°C.38,39 Therefore, the proliferation of germ cells may be affected by the increased temperature from the varicocele due to inhibition of one or more of these important enzymes. Hyperthermic injury is consistent with the reduction in spermatogonal num-bers observed in testis biopsy samples from patients with a varicocele.40 It is also likely that increased testicular temperature induces apoptosis in germ cells.41

Hypoxia

It has been hypothesized that the presence of a varicocele would be associated with venous stasis resulting in oxygen depletion in the testis. However, studies have failed to show evidence of hypoxia by testicular venous blood sampling.42,43 In addition,

TABLE 1. Incidence of Varicocele in Children

Reference Study Number of Patients Age Range

(Years)

Incidence (%)

Horner, 196010 1211 11–16 15.9

Oster, 19719 837 10–19 16.2

Steeno et al, 197611 4067 12–25 14.7

Yerokhin, 197912 10 000 10–17 12.4

Berger, 198013 586 10–17 9.0

D’Ottavio et al, 198114 5177 11–16 25.8

Total incidence 16.3

(3)

there is no significant difference in oxygen tension in testicular blood from animals with experimental varicoceles compared with controls.44

Adrenal Reflux

Reflux of blood down the testicular vein has been demonstrated by venography in patients with a var-icocele.45Therefore, there is potential for exposure of the testis to renal and adrenal metabolites via the testicular vein causing testicular dysfunction. How-ever, increased renal or adrenal metabolites at the level of the testis in varicocele patients has not been reported. Moreover, adrenalectomy in rhesus mon-keys with an experimental varicocele did not elimi-nate or diminish the effects of the varicocele.1Thus, adrenal reflux does not appear responsible for the testicular injury associated with the varicocele.

Endocrine Imbalances

A high intratesticular testosterone concentration (.20 ng/mL) is required to maintain spermatogen-esis in the rat.46Substantially decreased intratesticu-lar testosterone concentrations have been demon-strated in the rat experimental varicocele model with no apparent effect on serum testosterone concentra-tions.47 Other studies using experimental models of varicocele have shown that treatment with gonado-tropins result in improved testicular function.34 The results of human studies are mixed. Swerdloff and Walsh48(1975) found no difference in endocrine pro-files between varicocele patients and normal individ-uals. However, other studies have shown reduced testicular vein and serum testosterone levels in men with a varicocele, as well as an increase in serum testosterone levels after repair of the varicocele.49 –51 Some infertility patients with varicocele manifest an increase in pituitary secretion of luteinizing hormone (LH) in response to gonadotropin-releasing hormone (GnRH) challenge, implicating a compromise of the hypothalamic-pituitary-gonadal axis.52This is consis-tent with the impaired Leydig cell ultrastructure ob-served in testis biopsy samples in some patients with a varicocele, and Leydig cell function in rats with experimental varicoceles.40,47 These studies suggest that suboptimal concentrations of intratesticular tes-tosterone caused by altered blood flow, a dilutional effect due to increased venous volume, or compro-mised Leydig cell function could lower intratesticu-lar testosterone to a level that will not support nor-mal spermatogenesis in some patients with a varicocele.

Sertoli cell responsiveness to follicle-stimulating hormone (FSH) may be diminished in varicocele pa-tients due to an altered endocrine status or increased temperature of the testis. Stimulation of Sertoli cell function in experimentally induced varicocele mod-els results in improved semen parameters, suggest-ing that Sertoli cells are functionsuggest-ing suboptimally in the experimental varicocele model.34 Patients with varicocele have been shown to have altered levels of serum inhibin, which is produced by Sertoli cells.53In addition, histologic studies of testis biopsies from patients with varicoceles have demonstrated that germ cells in the adluminal compartment of the

sem-iniferous tubule are sloughed, a sign often associated with compromised Sertoli cell function.40,54 These studies suggest that insufficient endocrine support of Sertoli cell function may compromise spermatogen-esis in the varicocele testis.

Testicular Paracrine Imbalances

Spermatogenesis is a highly integrated process re-lying on intimate communication between different cell types of the testis.55–57Because coordinated secre-tion of paracrine factors is required for the cell-cell communication that leads to normal spermatogene-sis (Fig 2), testicular conditions that compromise the synthesis and/or secretion of paracrine factors (eg, increased testicular temperature, altered endocrine environment, etc) may prove to be detrimental to spermatogenesis.

Germ cells are isolated from the vascular system by tight junctional complexes formed between

(4)

cent Sertoli cells (ie, the blood-testis barrier). Sertoli cells secrete the proteins and other nutrients that are required for successful germ cell development in this isolated environment.58 One such nutrient is iron; Sertoli cells transport iron to the germ cells by syn-thesizing and secreting transferrin into the adluminal compartment of the seminiferous tubule.58 Trans-ferrin production has been shown to be correlated with spermatogenic efficiency in many different spe-cies, including humans.59 – 61Conditions that decrease testicular germ cell production, including varicocele, correlate with a decrease in transferrin production.62 Thus, compromise of Sertoli cell function resulting in limited production of essential nutrients, such as iron, may limit germ cell production.

Altered Blood Flow

Compared with many other tissues, blood pres-sure in the testicular capillaries and postcapillary venules is very low. The low pressure of this system makes it very sensitive to increases in pressure on the venous side. In fact, one study estimates that over 80% of a given increase in venous pressure would be transmitted to the testicular capillary bed.63 In-creased testicular venous pressure resulting in and/or accompanying the testicular varicocele could cause an increase in postcapillary venule pressure and thus dramatically increase the filtration volume of the postcapillary venules, potentially altering the composition of the interstitial space. This, in turn, could cause degenerative changes in cells that rely on this compartment, such as Leydig cells, peritubular myoid cells and Sertoli cells. The compromised func-tion of these cells would secondarily affect germ cell development. Increased blood flow, known to ac-company the varicocele, would increase the testicu-lar temperature due to inefficient cooling of the in-coming blood. The increased testicular temperature would exacerbate the effect of interstitial disruption by injuring germ cells directly. The result is a multi-factorial detrimental effect on testicular function.

Bilateral Effect

The cause of bilateral testicular dysfunction from a unilateral clinical varicocele is not known. Shafik and Bedeir64 (1980) demonstrated that pressure in the right testicular venous plexus is not elevated, as it is in the left testicular plexus, suggesting that reflux in the right testicular vein was not responsible for dys-function in the right testis. These investigators spec-ulate that circulation of blood from the left side via cross-communicating veins causes testicular injury on the right. Venographic studies have shown vari-ous routes of cross-anastomoses between left and right venous systems, although little or no contrast agent actually reaches the contralateral testis in these studies.23 In addition, a venographic study by Narayan et al18 (1981) found no evidence of cross-communication of venous blood, but showed retro-grade venous flow (ie, reflux) on the right in a high percentage of patients with left sided varicoceles. This suggests that direct reflux down the right tes-ticular vein, in addition to the left testes-ticular reflux, may cause the bilateral effect. Finally, the proximity

of an abnormally warm left testicle in the same scro-tum as the right testis is a possible explanation for bilateral elevation of testicular temperature.37

PATHOLOGY Histology

The histology of the varicocele testis shows that all the cell types and compartments of the testis can be involved. The varicocele-affected testis is often char-acterized by degeneration and sloughing of germ cells into the lumen of the tubule or by germ cells in various stages of maturation arrest.54,65– 68Sertoli cells also display ultrastructural changes and appear to slough portions of their adluminal cytoplasm.40,54 The basement membrane of the seminiferous tubule is often thickened.40 The effects on Leydig cells are quite variable, ranging from atrophy to hyperpla-sia.40,66 The venules and capillaries also display de-generative changes, such as endothelial hypertrophy, luminal narrowing, and thickening of the basement membranes.40 Importantly, these histologic changes are also characteristic of changes seen in the adoles-cent with a varicocele, though to less severe of a degree, and can occur as early as 12 years of age.40,69

Testicular Hypotrophy/Atrophy

The hallmark of testicular damage in the adoles-cent with a varicocele is a discrepancy in testicular size. Celsus described the association in the first century as “swollen veins, twisted over the testicle which becomes smaller than its fellow, inasmuch as its nutrition has become defective.”70Significant vol-ume loss in the adolescent with a varicocele has been noted in 77% of boys with 10% having a left testis one-fourth the size of the right testis.7

Testicular volume during preadolescence is rela-tively constant, as it is in adults. It is during the rapid growth of the testes, between 11 to 16 years of age, that a volume discrepancy between the two testes becomes clinically apparent in the adolescent with a varicocele.71 This increase in testicular volume dur-ing puberty is correlated with an increase in seminif-erous tubule size and germ cell number with the seminiferous tubules and germinal elements ulti-mately constituting 50% of the testicular mass.72,73 Therefore, it is not surprising that the loss of testic-ular volume in adolescents with left testictestic-ular vari-cocele is accompanied by a decrease in sperm count.74 The growth arrest associated with the ado-lescent varicocele is reversible in the majority of pa-tients.75–77

DIAGNOSIS Presentation

Varicoceles in adolescents are usually asymptom-atic and therefore the diagnosis is typically made at a routine physical examination. On occasion a pa-tient will present for evaluation of a scrotal mass or testicular discomfort, such as heaviness or a dull ache after standing all day.

(5)

examined standing in a warm room to relax the scro-tum and allow easier examination of the spermatic cord. The scrotum is first visually inspected for any obvious distentions around the spermatic cord; a visible varicocele is considered a large or Grade 3 varicocele. The scrotum, testes, and cord structures are then gently palpated. A palpable varicocele has been described as feeling like a bag of worms or a squishy tube. More subtle varicoceles may feel like a thickened or asymmetric cord. The nonvisible, but palpable varicocele, is considered to be moderate (Grade 2) in size. If a varicocele is not palpable, the patient performs a Valsalva maneuver which will produce a palpable impulse and distend the intras-crotal veins in a patient with a varicocele. A varico-cele detected only by Valsalva is considered a small (Grade 1) varicocele. After examining the patient in the standing position, the patient should be exam-ined supine. A thickened cord due to a varicocele should resolve in the supine position, whereas a thickened cord due to a lipoma will not change when the patient is supine.

Testicular size needs to be measured to determine if the varicocele is adversely affecting the testicle(s) and if repair of the varicocele is indicated. The vol-ume of a normal testis measures 1 to 2 mL in the prepubertal male. A volume greater than 3 mL usu-ally indicates the onset of puberty.78 From age 11 through 16 the volume of the testis increases from 2 to 16 mL.71Due to extensive individual variation in normal growth and development, testicular size is correlated best with Tanner Stage, growth velocity, and bone age rather than chronological age.79,80The left testis has been noted to be smaller than the right, but the difference is not statistically significant.79,81 Ethnic variations in testis size have also been docu-mented, with smaller testes noted in Asian men when compared with whites, and no significant dif-ference in testicular size noted between black and white males.79,82 These variations in laterality and ethnicity need to be taken into account when mea-suring testicular size.

A number of methods have been used to measure the size of the testis. These include visual compari-son, rulers, calipers, comparative ovoids (Prader Or-chidometer), punched-out elliptical rings (Takihara Orchidometer), and ultrasound. Measurements of testicular length, width, and depth can be substituted into the formula of a prolate ellipsoid to estimate testicular volume [VOL (mL)5.5233L W D].81All methods of measurement tend to overestimate the actual size of small volume testes and underestimate large volume testes.83Behre and associates compared ultrasound measurement and actual testicular vol-ume determined by weight and volvol-ume displace-ment in 14 testes from patients at autopsy.84A high correlation (r5.992) between ultrasound and actual volume was noted and was shown to be highly re-producible. The Prader Orchidometer was shown to correlate with ultrasound measurement in 256 pa-tients (r5.91), though the degree of correlation was dependent upon the investigator’s clinical experi-ence.84In a clinical study of 22 male adolescents with a varicocele, 24% of patients with growth arrest

would have been missed if measured by Prader Or-chidometer alone, and three patients felt to have a significant size discrepancy (.2 mL) by Prader Or-chidometer measurements were found to be normal by ultrasound volume estimate.85These findings in-dicate that clinical estimates of testicular size by the Prader Orchidometer are not as accurate or repro-ducible as those determined by ultrasound examina-tion. Accurate measurement is important because operative decisions rest in the balance.

There is significant disagreement as to what con-stitutes a significant size discrepancy justifying sur-gical intervention.75,76It is apparent in the literature that testicular ultrasound is the most accurate and reproducible method to assess testicular volume and significant testicular size variations. A volume differ-ence of less than 2 mL can be due to the measure-ment technique alone. Therefore, size variation of greater than 2 mL by ultrasound is currently the best indicator of testicular damage and should serve as the minimal requirement for surgical repair of the adolescent varicocele.

Venography

Venography is touted as the gold standard for diagnosing varicoceles in adults, but has a limited role with adolescents. This stems from the difference in presentation in these two populations. Older pa-tients are usually evaluated for infertility and a sub-tle varicocele is sometimes sought to explain abnor-mal semen parameters, whereas adolescents are typically recognized with a clinically apparent vari-cocele. Occasionally venography is performed in the adolescent to confirm the small or subclinical varico-cele in cases of a confusing presentation such as scrotal pain or testicular atrophy of unknown etiol-ogy. In addition, venography is sometimes per-formed in conjunction with embolization as treat-ment of a varicocele in the adolescent.

Other Techniques

Doppler ultrasound, thermography, and scrotal scintigraphy have been used to diagnose varicoceles in adults.86,87 These techniques are nonspecific for diagnosing a varicocele and, for the same reason as venography, are not generally used in the diagnosis of the adolescent varicocele.

Potential Techniques

Methods to assess reproductive function such as semen analysis, testis biopsy, and fine needle aspira-tion with flow cytometry are not recommended for the adolescent with a varicocele. However, in the future, measuring altered levels of paracrine mole-cules of testicular origin may provide a diagnostic tool for assessing testicular function in the adolescent with a varicocele.

CONTROVERSIES IN MANAGEMENT Controversies on Varicocele Size

What is the relationship of varicocele size to ad-verse effects on the testis and treatment results? It

(6)

(1970) that the size of a varicocele does not correlate with adverse effects of a varicocele. They showed good results after varicocele repair whether the size was grade 1, 2, or 3. Vereecken and Boeckx89 (1986) looked at the semen analysis in 374 patients who underwent a varicocele repair. Preoperatively, se-men analyses did not correlate with varicocele size. Postoperatively, all semen parameters, in general, seemed to improve and left testicular volume in-creased. Lyon and associates7 (1982) showed that there was no correlation to varicocele grade and testicular size in 30 adolescents with a left sided varicocele.

In contrast, a large screening of 4067 adolescents by Steeno and associates11 detected approximately 598 students (14.7%) with a varicocele of which an abnormal testis was noted in 34% of those with a moderate size varicocele compared with 81% of those with a large varicocele. Fariss and associates90 (1981) performed a semen analysis on 131 adult pa-tients who were found to have a varicocele on a routine physical examination. They showed that there was a greater percentage of men with a sperm concentration of less than 20 million per mL in those with a large or medium sized varicocele when com-pared with those with a small varicocele. Others have shown that there is an inverse relationship be-tween preoperative semen values and varicocele size and that the larger the varicocele, the greater the improvement in semen parameters after varicocele repair.91,92 Presumptively, the parallel argument in the adolescent is that the larger the varicocele, the greater the damage to the germ cells and, conse-quently, the greater the testicular atrophy.

Effects of Varicocele on Testicular Function Over Time

There is good evidence that the duration of a var-icocele causes progressive adverse effects on the tes-tis. Chehval and Porcell2 (1992) performed semen analyses in 13 men with varicoceles and then re-evaluated them 9 to 96 months later. They showed a significant deterioration in their follow-up semen analyses. Okuyama and colleagues93(1988) showed that of 11 adolescents with a varicocele and no initial testicular atrophy, 3 of 5 (60%) who remained un-treated developed atrophy, whereas none of the 6 who underwent immediate varicocele repair devel-oped testicular atrophy on follow-up. Finally, Gorelick and Goldstein3(1993) reviewed the records of 1099 infertile men and found 98 who had second-ary infertility (ie, had a child and then developed infertility). A varicocele was detected in 35% of men with primary infertility and 81% of men with sec-ondary infertility. All of these studies suggest that a varicocele can cause progressive testicular damage over time.

Which Adolescents With Varicoceles Should Undergo Therapy?

The varicocele is the most common correctable cause of adult male factor infertility.94 Numerous retrospective studies have demonstrated an im-provement in both semen quality and pregnancy rates after treatment; a summary of many of these

studies shows that approximately 66% of patients will have an improvement in semen quality and 43% of the partners will become pregnant.6 At least 6 studies have compared surgical or percutaneous treatment of varicoceles with medical or no treat-ment of varicoceles.6 The weighted mean of these studies shows that 30% of adult patients who un-dergo surgical or percutaneous treatment of the var-icocele will result in a pregnancy versus 16% who undergo medical or no therapy. A recent random-ized controlled study noted a 10% pregnancy rate after a year of observation in a nonoperated control group compared with a 60% pregnancy rate during the same time period in a group that underwent immediate varicocele repair.95

Historically, the adolescent with a varicocele was left untreated, because its significance in regards to fertility were and remain unknown. The observation by Kass and Belman75that testicular growth retarda-tion associated with a moderate to large varicocele was partially reversed by early treatment has led to a more aggressive approach to the adolescent with a varicocele. Unfortunately, left testicular hypotrophy by itself will not predict all of the subpopulation of adolescents with varicoceles who will subsequently develop infertility. Consequently, a number of ques-tions arise concerning which, if any, adolescents should undergo surgery to correct the varicocele.

Because of difficulty collecting semen specimens and the lack of normal standards for semen param-eters in adolescents, other techniques have been ex-plored for identifying adolescents with varicocele induced testicular damage. GnRH stimulation stud-ies have demonstrated exaggerated FSH and LH re-sponses to GnRH stimulation in adult and adolescent males with a varicocele.96 An elevated LH and FSH response to GnRH stimulation was felt to indicate significant testicular dysfunction, and this was noted in 30% of adolescent patients with varicoceles.96The abnormal response was not associated with left tes-ticular volume loss. Although this test provides fur-ther evidence of testicular damage, it is expensive, requires multiple blood samplings, and would re-quire repetitive studies to evaluate for progressive dysfunction if it were initially normal. The associa-tion of an abnormal GnRH stimulaassocia-tion test with subsequent infertility is not established. Thus, at present, we do not advise a GnRH test as a method to select patients for surgical management.

(7)

best measurement, and a left testis 2 mL smaller than the right is statistically significant.85 Although we have no proof of improved fertility, catch-up growth of the left testis will occur in 80% of those patients who undergo varicocele repair.75

A small number of adolescents will have bilateral varicoceles, significant discomfort related to the var-icocele, and very large varicoceles that may cause parental concern. Adolescents with a large varicocele have traditionally been considered to be at risk for testicular dysfunction.7The incidence of postpuber-tal males at risk with a large varicocele is approxi-mately 6.8% when calculated as a weighted mean from four large surveys on varicoceles among ado-lescents.9 –12Given the associated infertility data, the decision for surgery in young males with bilateral varicoceles, a large varicocele, or scrotal discomfort due to a varicocele, must be individualized.

In boys with varicoceles and bilateral normal size testes, the decision to perform surgery is much more difficult. In these patients, serial ultrasounds per-formed every 6 to 12 months will identify the 12% to 40% who will develop significant testicular growth arrest. If concern remains, a semen analysis can be performed when the adolescent reaches an appropri-ate age.

In summary, because the treatment is relatively inexpensive and safe, a varicocele repair in adoles-cents or pediatric patients with a varicocele is recom-mended by most specialists for the following: 1. A greater than 2 mL difference in testicular

vol-ume as noted on serial ultrasonographic examina-tions, or

2. A two standard deviation decrease in testicular size when compared with normal testicular growth curves, or

3. Scrotal pain.

Finally, some would also consider a varicocele re-pair in young males with a large or bilateral varico-celes.

TREATMENT Techniques

Multiple techniques for treating a varicocele have been well described in the literature and will not be

repeated here. A summary of their advantages, dis-advantages, and complication rates are shown in Table 2.2,6,76,97–106,113

Persistence and Recurrence Rates

If the decision to perform surgery in the adolescent with a varicocele is not hard enough, dealing with a persistent or recurrent varicocele is even more diffi-cult. The persistent varicocele, which in some cases may be a recurrent varicocele, is not uncommon with rates of 9% to 16% after varicocelectomy in adoles-cents.76,105,106 This persistence rate is purportedly higher in adolescents as compared with adults after varicocele repair and, thus, implies different techni-cal concerns in repairing the adolescent varicocele compared with the adult.107However, the weighted mean of these reports suggests a 13.6% persistence rate in adolescents, that is little different than the 15% persistence (recurrence) rate after repair by the retroperitoneal approach in the adult, as shown in Table 2.76,105,106

Persistent varicoceles are often due to an unrecog-nized parallel communicating internal spermatic vein. Distal collaterals via pelvic veins such as cre-masteric, deferential, and suprapubic and retropubic cross-over veins, occur less commonly.108 The high persistence rates and location of the culprit vein have been studied extensively by intraoperative postliga-tion internal spermatic venography, which was de-veloped to diminish the persistence rate. Several in-vestigators have intraoperatively identified proximal collaterals in 16% to 39% of adolescent patients by this technique.107The persistence rate on follow-up in adolescent patients who underwent varicocelectomy with intraoperative venography to identify and li-gate proximal collaterals is approximately 6%.109,110

This high persistence rate has resulted in a variety of other radiologic and surgical procedures to correct the varicocele and diminish this complication. These procedures include embolization of the internal sper-matic vein, microsurgical varicocelectomy, and the retroperitoneal (ie, Palomo) approach with both ve-nous and arterial ligation. Embolization as treatment of the adolescent varicocele is not used as commonly as in the adult and has a high persistence rate (26%).111 Embolization may have a role in

conjunc-TABLE 2. Treatment Options

Technique Complication Rate Cost* Failure Rate Comments References

Conventional inguinal 3–8.6% Hydrocele $ 16% Recurrence (adolescents) 9% Recurrence (adults)

Easiest technique 2, 97–100

Microscopic inguinal 0% Hydrocele $$ 0.6% Recurrence Very low complication rate 104 Microscopic subinguinal 0.8% Hydrocele $ 2.1% Recurrence Can be done under local

anesthesia; fast recovery 102

Retroperitoneal 7.2% Hydrocele $ 13.6% Recurrence (adolescents, artery sparing)

,2% Recurrence (adolescents, artery taking)

15% Recurrence (adults)

Most common method of pediatric urologists

76, 103, 105, 106, 113

Laparoscopic Similar to retroperitoneal $$$ 15% Recurrence Fast recovery, but potential for serious injury

101

Embolization 11% Overall rate† $$$ 5% Recurrence and 27% nonocclusion rate, for a 31% overall failure rate

Fast recovery 6

* Relative costs estimated on necessity for anesthesia, time in operating room, and equipment.

(8)

tion with surgery or in treating the postsurgical per-sistent varicocele.102 The procedure in adults associ-ated with the lowest persistence rate is the microsurgical inguinal or subinguinal approach (Ta-ble 2). In a small study, the microsurgical technique was done in 22 boys with no recurrence or compli-cations.112 Additional studies need to be done using microsurgical techniques.

Atrassi and colleagues recently reported their re-sults with the Palomo procedure that involves liga-tion of the testicular artery and internal spermatic veins in the retroperitoneum.113 Their persistence rate of ,2% is low and is consistent with other reports using this surgical approach in adolescents. Their hypothesis for the decreased persistence rate is that collateral internal spermatic veins intimately as-sociated with the internal spermatic artery are li-gated using this technique. These collaterals may be difficult to identify even with venography and only become significant after selective ligation of the larger primary internal spermatic veins. Testicular atrophy is uncommon with the Palomo technique (with arterial ligation).113,114 In addition, catch-up growth of the testis in the successfully treated vari-cocele has been noted, whereas persistence of the varicocele resulted in lack of testicular growth.113 Therefore, a failed operation to correct the varicocele appears to be more detrimental to the testis than arterial disruption.

The major objection to arterial ligation during var-icocele repair is that the long-term effect of arterial ligation on spermatogenesis is unknown. However, the reversal of growth arrest, and the absence of left testicular atrophy after internal spermatic artery li-gation imply that collateral arterial blood supply via the deferential and cremasteric arteries is sufficient for the growth and development of the testis. A caveat with this approach is that the Palomo proce-dure would not be appropriate in patients with pre-vious inguinal surgery, because the cremasteric and deferential arterial circulation to the testis may be compromised. Likewise, subsequent vasectomy in these patients must be avoided because ligation of the vasal artery could lead to atrophy of the testis in the absence of blood supply via the internal testicular artery.

At present, high retroperitoneal ligation of the in-ternal spermatic artery and veins is the procedure with the lowest persistence rates in the adolescent literature. In a survey of 23 pediatric urologists, ret-roperitoneal ligation with taking the testicular artery was the most common treatment for the adolescent varicocele (Skoog and Pryor, unpublished results, 1995). This is in distinct contrast to the microscopic inguinal or subinguinal approach used most com-monly in a survey of 9 adult male infertility special-ists (Skoog and Pryor, unpublished results, 1995). Given the uncertainties of mass retroperitoneal liga-tion of artery and vein, and the lower rate of hydro-cele formation and similar rates of recurrence of mi-crosurgical techniques, pediatric urologists should consider using the microscopic inguinal or subingui-nal approach.

PSYCHOLOGICAL IMPACT

The occurrence and diagnosis of a varicocele in the adolescent male has potential psychological conse-quences. The majority of boys are not aware of its presence; 94% of school boys and 78% of college students when questioned at the time of clinical dis-covery did not know a varicocele was present.11 In this same study, when these young men were in-formed of the presence of the varicocele and its po-tential effects, of which they were unaware, a num-ber of psychological problems were encountered. Depressive reactions, concentration difficulties, loss of confidence in medicine, and anxiety related to fertility and potency were reported. These untoward psychological factors were present in 29% to 36% of nonoperated patients and 23% to 27% of postopera-tive patients.11

This experience suggests that each patient and his parents be approached in a cautious manner. The parents know their son and his psychological make-up. Their concerns and recommendations in regards to the method of delivery of the information to their child should be elicited. The documentation that early surgery in the adolescent will prevent later fertility problems is lacking and discussion with the adolescent of a possible fertility disorder at adult age risks possible psychological reactions of sexual and genital inferiority.11 The only known outcome is the effect of surgery on subsequent testicular growth and this should be all that is stressed.

SUMMARY/CONCLUSIONS

Left testicular growth arrest (hypotrophy) is seen in association with the varicocele. The mechanism responsible for the growth arrest is undefined. It most likely represents a combination of effects re-lated to thermoregulation, temperature dependent enzyme systems, intratesticular hormonal concentra-tions, and alterations in paracrine interactions in-volved in spermatogenesis. All of these theories are based on the assumption that the varicocele is asso-ciated with an abnormality of blood flow. Growth arrest is reversible and catch-up growth of the left testis occurs after surgical correction of the varico-cele. The relationship of testicular hypotrophy and its reversibility to subsequent fertility is unknown; however, clinical studies suggest that the improved growth of the testis, increase in total sperm counts, and improvement in other seminal parameters will be beneficial to ultimate fertility.

The best clinical indication of significant testicular dysfunction related to the varicocele is growth arrest. The measurement of a 2 mL or greater size discrep-ancy between the left and right testis in the adoles-cent constitutes significant growth arrest in the left testis and is the main indication for surgery in the adolescent. Measuring testicular volume is most ac-curately performed with ultrasound. A decrease in testicular growth by two standard deviations from growth curves, scrotal pain, or a large (Grade 3) varicocele are other reasons to consider varicocele repair.

(9)

ado-lescents than adults after surgery, our review sug-gests similar persistence rates of 15% when a retro-peritoneal approach to repair is used. At present, the procedure with the reported lowest persistence rates (1% to 2%) in adolescents is the high retroperitoneal ligation of the testicular artery and vein. The effects of internal spermatic artery ligation on spermatogen-esis are unknown. The microsurgical inguinal or sub-inguinal approach with its low rate of hydrocele formation and low persistence rate deserves to be considered and used by pediatric urologists. The objectives of promoting testicular growth and possi-bly improving fertility later in life must take into consideration the psychological impact of these is-sues on the adolescent.

FUTURE DIRECTIONS

Because a minority of adult males with a varico-cele are infertile, an important advance in the treat-ment of the adolescent varicocele will be the ability to select pediatric patients who will develop subse-quent male factor infertility. The present criteria of delayed testicular growth does not predict future infertility. Future studies need to focus on identify-ing factors required for meiosis and germ cell matu-ration that can be measured in pediatric patients, in body fluids other than semen. Candidate factors in-clude inhibin, PmodS, and Mullerian inhibiting sub-stance. Studies on blood flow patterns and investi-gating the basis of spermatogenic dysfunction at the cellular and molecular level in the varicocele patient need to continue. These investigations should help us more fully understand the pathophysiology of testicular dysfunction caused by the varicocele, and provide us with insight on developing new strategies for the early diagnosis and treatment of this common problem in adolescents.

ACKNOWLEDGMENTS

We are grateful to Dr John Barry at the Oregon Health Sciences Center and Dr Michael Caldwell and David Hunter at the Uni-versity of Minnesota Medical School for their helpful comments and review of this manuscript.

REFERENCES

1. Harrison RM, Lewis RW, Roberts JA. Pathophysiology of varicocele in nonhuman primates: long-term seminal and testicular changes. Fertil Steril. 1986;46:500 –510

2. Chehval MJ, Purcell MH. Deteriorations of semen parameters over time in men with untreated varicocele: evidence of progressive testicular damage. Fertil Steril. 1992;57:174 –177

3. Gorelick JI, Goldstein M. Loss of fertility in men with varicocele. Fertil Steril. 1993;59:613– 616

4. Witt MA, Lipschultz LI. Varicocele: a progressive or static lesion? Urology. 1993;42:541–543

5. Saypol DC. Varicocele. J Androl. 1981;2:61–71

6. Pryor JL, Howards SS. Varicocele. Urol Clin North Am. 1987;14:499 –513 7. Lyon RP, Marshall S, Scott MP. Varicocele in childhood and adolescence: implication in adulthood infertility? Urology. 1982;19: 641– 644

8. Sawczuk IS, Burbige KA, Hensle TW. Asymptomatic varicocele in an infant. Clin Pediatr (Phila). 1985;24:285–286

9. Oster J. Varicocele in children and adolescents. An investigation of the incidence among Danish school children. Scand J Urol Nephrol. 1971;5: 27–32

10. Horner JS. The varicocele. A survey amongst secondary schoolboys. Medical Officer. 1960;104:377–381

11. Steeno O, Knops J, DeClerck L, Adimoelja A, van de Voorde H.

Pre-vention of fertility disorders by detection and treatment of varicocele at school and college age. Andrologia. 1976;8:47–53

12. Yerokhin AP. Classification and frequency of varicocele in children. Klin Khir. 1979;6:45– 46

13. Berger OG. Varicocele in adolescence. Clin Pediatr (Phila). 1980;19: 810 – 811

14. D’Ottavio G, et al. Il varicocele idiopatico: considerazioni epidemio-logiche e pathogenetiche. In: D’Ottavio G, Pozza D, eds. Andrologia Chirugica. Rome, Italy: Borla; 1981:77

15. Lee LM, Johnson HW, McLoughlin MG. Microdissection and radio-graphic studies of the arterial vasculature of the human testes. J Pediatr Surg. 1984;19:297–301

16. Jarow JP. Intratesticular arterial anatomy. J Androl. 1990;11:255–259 17. Palomo A. Radical cure of varicocele by a new technique: Preliminary

report. J Urol. 1949;61:604 – 607

18. Narayan P, Amplatz K, Gonzalez R. Varicocele and male subfertility. Fertil Steril. 1981;36:92–97

19. Wishahi MM. Detailed anatomy of the internal spermatic vein and the ovarian vein. Human cadaver study and operative spermatic venography: clinical aspects. J Urol. 1991;145:780 –784

20. Shafik A, Moftah A, Olfat S, Mohi el Din M, El Sayed A. Testicular veins: anatomy and role in varicocelogenesis and other pathologic conditions. Urology. 1990;35:175–182

21. Hill JT, Green NA. Varicocele: a review of radiologic and anatomical features in relation to surgical treatment. Br J Surg. 1977;64:747–752 22. Hunter DW, King NJ, Aeppil DM, et al. Spermatic vein occlusion with

hot contrast material: angiographic results. J Vasc Interv Radiol. 1991;2: 507–515

23. Etriby AA-E, Ibrahim A-AA, Mahmoud KZ, Elhaggar S. Subfertility and varicocele. I. Venogram demonstration of anastomosis sites in subfertile men. Fertil Steril. 1975;26:1013–1017

24. Saypol DC, Lipshultz LI, Howards SS. Varicocele, In: Lipshultz, LI, Howards, SS, eds. Infertility in the Male. New York, NY: Churchhill Livingstone; 1983

25. Ahlberg NE, Bartley O, Chidekel N. Retrograde contrast filling of the gonadal vein: a roentgenologic and anatomical study. Acta Radiol. 1965; 3:385–392

26. Ahlberg NE, Bartley O, Chidekel N, Fritjofsson A. Phlebography in varicocele scroti. Acta Radiol. 1966;4:517–528

27. Ahlberg NE, Bartley O, Chidekel N. Right and left gonadal veins: an anatomical and statistical study. Acta Radiol. 1966;4:593– 601

28. Coolsaet BL. The varicocele syndrome: venography determining the optimal level for surgical management. J Urol. 1980;124:833– 839 29. Saypol DC, Howards SS, Turner TT, Miller ED Jr. Influence of surgically

induced varicocele on testicular blood flow, temperature, and histology in adult rats and dogs. J Clin Invest. 1981;68:39 – 45

30. Beinart C, Sniderman KW, Tamura S, Vaughan ED, Sos TA. Left renal vein to inferior vena cava pressure relationship in humans. J Urol. 1982;127:1070 –1071

31. Zerhouni EA, Siegelman SS, Walsh PC, White RI. Elevated pressure in the left renal vein in patients with varicocele: preliminary observations. J Urol. 1980;123:512–513

32. White RI Jr, Kaufman SL, Barth KH, Kadir S, Smyth JW, Walsh PC. Occlusion of varicoceles with detachable ballons. Radiology. 1981;139: 327–334

33. Kay R, Alexander NJ, Baugham WL. Induced varicocele in rhesus monkeys. Fertil Steril. 1979;31:195–199

34. Sofikitis N, Takahashi C, Kadowaki H, et al. Surgical repair versus medical treatment of varicocele in the rat: pharmacological manipula-tion of the varicocelized testicle. Eur Urol. 1992;22:44 –52

35. Harrison RG. Effect of temperature on the mammalian testis. In: Hamilton DW, Greep RO, eds. Handbook of Physiology, V. Washington, DC: American Physiological Society; 1975

36. Zorgniotti AW. Testis temperature, infertility, and the varicocele para-dox. Urology. 1980;16:7–10

37. Goldstein M, Eid J-F. Elevation of intratesticular and scrotal skin surface temperature in men with varicocele. J Urol. 1989;142:743–745 38. Fujisawa M, Yoshida S, Kojima K, Kamidono S. Biochemical changes in

testicular varicocele. Arch Androl. 1989;22:149 –159

39. Fujisawa M, Yoshida S, Matsumoto O, Kojima K, Kamidono S. Deoxyri-bonucleic acid polymerase activity in the testes of infertile men with varicocele. Fertil Steril. 1988;50:795– 800

40. Hienz HA, Voggenthaler J, Weissbach L. Histological findings in testes with varicocele during childhood and their therapeutic consequences. Eur J Pediatr. 1980;133:139 –146

(10)

internal spermatic veins of subfertile men with varicocele. Fertil Steril. 1969;20:365–369

43. Netto NR Jr, Lemos GC, De Goes GM. Varicocele: relation between anoxia and hypospermatogenesis. Int J Fertil. 1977;22:174 –178 44. Turner TT, Jones CE, Roddy MS. Experimental varicocele does not

affect the blood-testis barrier, epididymal electrolyte concentrations, or testicular blood gas concentrations. Biol Reprod. 1987;36:926 –932 45. Comhaire F, Vermuelen A. Varicocele sterility: cortisol and

catecolemi-nes. Fertil Steril. 1974;25:88 –95

46. Zirkin BR, Santulli R, Awoniyi CA, Ewing LL. Maintenance of advanced spermatogenic cells in the adult rat testis: quantitative relationship to testosterone concentration within the testis. Endocrinology. 1989;124: 3043–3049

47. Rajfer J, Turner TT, Rivera F, Howards SS, Sikka SC. Inhibition of testicular testosterone biosynthesis following experimental varicocele in rats. Biol Reprod. 1987;36:933–937

48. Swerdloff RS, Walsh PC. Pituitary and gonadal hormones in patients with varicocele. Fertil Steril. 1975;26:1006 –1012

49. Ando S, Giacchetto C, Colpi G, et al. Plasma levels of 17-OH-progesterone and testosterone in patients with varicoceles. Acta Endo-crin (Copenh). 1983;102:463– 469

50. Ando S, Giacchetto C, Beraldi E, Panno ML, Carpino A, Brancati C. Progesterone, 17-OH-progesterone, androstenedion and testosterone plasma levels in spermatic venous blood of normal men and varicocele patients. Horm Metab Res. 1985;17:99 –103

51. Su L-M, Goldstein M, Schlegel PN. The effect of varicocelectomy on serum testosterone levels in infertile men with varicoceles. J Urol. 1995; 154:1752–1755

52. Bickel A, Dickstein G. Factors predicting the outcome of varicocele repair for subfertility: the value of the luteinizing hormone-releasing hormone test. J Urol. 1989;142:1230 –1234

53. Plymate SR, Paulsen CA, McLachlan RI. Relationship of serum inhibin levels to serum follicle stimulating hormone and sperm production in normal men and men with varicoceles. J Clin Endocrinol Metab. 1992;74: 859 – 864

54. Cameron DF, Snydle FE, Ross MH, Drylie DM. Ultrastructural alter-ations in the adluminal testicular compartment in men with varicocele. Fertil Steril. 1980;33:526 –533

55. Skinner MK. Cell-Cell interactions in the testis. Endocr Rev. 1991;12: 45–77

56. Krummen LA, Moore A, Woodruff TK, et al. Localization of inhibin and activin binding sites in the testis during development by in situ ligand binding. Biol Reprod. 1994;50:734 –744

57. Han IS, Sylvester SR, Kim KH, et al. Basic fibroblast growth factor is a testicular germ cell product which may regulate Sertoli cell function. Mol Endocrinol. 1993;7:889 – 897

58. Griswold MD, Morales C, Sylvester SR. Molecular biology of the Sertoli cell. Oxford Rev Reprod Biol. 1988;10:124 –161

59. Gilmont RR, Senger PL, Sylvester SR, Griswold MD. Seminal transferrin and spermatogenic capacity in the bull. Biol Reprod. 1990;43:151–157 60. Barthelemy C, Khalfoun B, Guillaumin JM, Lecomte P, Bardos P.

Sem-inal fluid transferrin as an index of gonadal function in men. J Reprod Fertil. 1988;82:113–118

61. Mallea L, Mas J, Padron RS, Diaz JW. Transferrin in seminal plasma of fertile and infertile men. Andrologia. 1988;20:15–20

62. Yoshida K-I, Nakame Y, Uchijima Y. Seminal plasma transferrin con-centration in normozoospermic fertile men and oligospermic men as-sociated with varicocele. Int J Fertil. 1988;33:432– 436

63. Sweeney TE, Rozum JS, Desjardins C, Gore RW. Microvascular preasure distribution in the hamster testis. Am J Physiol. 1991;260:H1581–1589 64. Shafik A, Bedeir GAM. Venous tension patterns in cord veins. I. In

normal and varicocele individuals. J Urol. 1980;123:383–385

65. Etriby A, Girgis SM, Hefnawy H, Ibranim AA. Testicular changes in subfertile males with varicocele. Fertil Steril. 1967;18:666 – 671 66. Dubin L, Hotchkiss RS. Testis biopsy in subfertile men with varicocele.

Fertil Steril. 1969;20:51–57

67. Kass EJ, Chandra RS, Belman AB. Testicular histology in the adolescent with a varicocele. Pediatrics. 1987;79:996 –998

68. Wang Y-X, Lei C, Dong S-G, Chandley AC, MacIntyre M, Hargreave TB. Study of bilateral histology and meiotic analysis in men undergoing varicocele ligation. Fertil Steril. 1991;55:152–155

69. Pozza D, D’Ottavio G, Masci P, Coia L, Zappavigna D. Left varicocele at puberty. Urology. 1983;22:271–274

70. Spencer WG. Celsus de medicina (With an English Translation). Cam-bridge, Mass: Harvard University Press; 1938

71. Hall JG, Foster-Iskenius UG, Allanson JE. Handbook of Normal Physical Measurements. Oxford, NY: Oxford University Press; 1989:325 72. Rey RA, Campo SM, Bedecarras P, Nagle CA, Chemes HE. Is infancy a

quiescent period of tesicular development? Histological, morphometric, and functional study of the seminiferous tubules of the cebus monkey from birth to the end of puberty. J Clin Endocrinol Metab. 1993;76: 1325–1331

73. Johnson L, Petty CS, Neaves WB. A comparative study of daily sperm production and testicular composition in humans and rats. Biol Reprod. 1980;22:1233–1243

74. Haans LCF, Laven JSE, Mali WPTM, Velde ER, Wensing CJG. Testis volumes, semen quality, and hormonal patterns in adolescents with and without a varicocele. Fertil Steril. 1991;56:731–736

75. Kass EJ, Belman AB. Reversal of testicular growth failure by varicocele ligation. J Urol. 1987;137:475– 476

76. Reitelman C, Burbige KA, Sawczuk IS, Hensle TW. Diagnosis and surgical correction of the pediatric varicocele. J Urol. 1987;138: 1038 –1040

77. Laven JS, Haans LC, Mali WP, et al. Effects of varicocele treatment in adolescents: a randomized study. Fertil Steril. 1992;58:756 –762 78. Zachmann M, Prader A, Kind HP, Hafliger H, Budliger A. Testicular

volume during adolescence. Cross sectional and longitudinal studies. Helv Pediatr Acta. 1974;29:61–72

79. Daniel WA, Feinstein RA, Howard-Peebles P, Baxley WD. Testicular volumes of adolescents. J Pediatr. 1982;101:1009 –1012

80. Sizoneko PC, Schindler AM, Lecoultre C, et al. Clinical evaluation and management of testicular disorders before puberty. In: Burger H, de Kretser D, eds. The Testis. 2nd ed. New York, NY: Raven Press; 1989:388 81. Sayfan JS, Soffer Y, Manor H, et al. Varicocele in youth: a therapeutic

dilemma. Ann Surg. 1988;207:223–227

82. Diamond JM. Variation in human testis size. Nature. 1986;320:488 83. Takihara H, Sakatoku J, Fujii M, et al. Significance of testicular size

measurement in andrology: a new orchiometer and its clinical applica-tion. Fertil Steril. 1983;39:835– 840

84. Behre HM, Nashan D, Nieschlag E. Objective measurement of testicular volume by ultrasonography: evaluation of the technique and compari-son with orchidometer estimates. Int J Androl. 1989;12:395– 403 85. Costabile RA, Skoog SJ, Radowich M. Testicular volume assessment in

the adolescent with a varicocele. J Urol. 1992;147:1348 –1350

86. Hirsh AV, Kellet MJ, Robertson G, Pryor JP. Doppler flow studies, venography and thermography in the evaluation of varicoceles of fertile and subfertile men. Br J Urol. 1980;52:560 –565

87. Wheatley JK, Fajman WA, Witten FR. Clinical experience with the radioisotope scan as a screening method for the detection of subclinical varicoceles. J Urol. 1982;128:57–59

88. Dubin L, Amelar RD. Varicocele size and results of varicocelectomy in selected subfertile men with varicocele. Fertil Steril. 1970;21:606 – 609 89. Vereecken RL, Boeckx G. Does fertility improvement after varicocele

treatment justify preventive treatment at puberty? Urology. 1986;28: 122–126

90. Fariss BL, Fenner DK, Plymate SR, Brannen GE, Jacob WH, Thomason AM. Seminal characteristics in the prescence of a varicocele as com-pared with those of expectant fathers and prevasectomy men. Fertil Steril. 1981;35:325–327

91. Tinga DJ, Siemen J, Bruijnen CLAH, Kremer J, Mensink HJ. Factors related to semen impovement and fertility after varicocele operation. Fertil Steril. 1984;41:404 – 410

92. Steckel J, Dicker AP, Goldstein M. Relationship between varicocele size and response to varicocelectomy. J Urol. 1993;149:769 –771

93. Okuyama A, Nakamura M, Namiki M, et al. Surgical repair of varico-cele at puberty: preventive treatment for fertility improvement. J Urol. 1988;139:562–564

94. Greenberg SH, Lipshultz LI, Wein A. Experience with 425 subfertile male patients. J Urol. 1978;119:507–510

95. Madgar I, Weissenberg R, Lunenfeld B, Karasik A, Goldwasser B. Controlled trial of high spermatic vein ligation for varicocele in infertile men. Fertil Steril. 1995;63:120 –124

96. Kass EJ, Freitas JE, Salisz JA, Steinert BW. Pituitary gonadal dysfunction in adolescents with varicocele. Urology. 1993;42:179 –181

97. Dubin L, Amelar RD. Varicocelectomy: 986 cases in a 12 year study. Urology. 1977;10:446 – 449

98. Ross LS, Ruppman N. Varicocele vein ligation in 565 patients under local anesthesia: a long-term review of technique, results and compli-cations in light of proposed management by laparoscopy. J Urol. 1993; 149:1361–1363

99. Kass EJ, Marcol B. Results of varicocele surgery in adolescents: a com-parison of techniques. J Urol. 1992;148:694 – 696

100. Cvitanic OA, Cronan JJ, Sigman M, Landau ST. Varicoceles: postoper-ative prevalence—a prospective study with color Dopler US. Radiology. 1993;187:711–714

(11)

M, ed. Surgery of Male Infertility. Philadelphia, PA: WB Saunders Company; 1995

102. Marmar JL, Kim Y. Subinguinal microsurgical varicocelectomy: a tech-nical critique and statistical analysis of semen and pregnancy data. J Urol. 1994;152:1127–1132

103. Szabo R, Kessler R. Hydrocele following internal spermatic vein ligation: a retroperitoneal study and review of the literature. J Urol. 1984;132:924 –925

104. Goldstein M, Gilbert BR, Dicker AP, Dwosh J, Gnecco C. Microsurgical inguinal varicocelectomy with delivery of the testis: an artery and lymphatic sparing technique. J Urol. 1992;148:1808 –1811

105. Holschneider AM, Butenandt O, Schuster L, et al. Operative therapy of varicocele in childhood. Z Kinderchir. 1978;24:252–256

106. Gorenstein A, Katz S, Schiller M. Varicocele in children: to treat or not to treat. Venographic and manometric studies. J Pediatr Surg. 1986;21: 1046 –1050

107. Levitt S, Gill B, Katlowitz N, Kogan SJ, Reda E. Routine intraoperative post-ligation venography in the treatment of the pediatric varicocele. J Urol. 1987;137:716 –718

108. Gill B, Kogan SJ, Maldonado J, Reda E, Levitt SB. Significance of

intraoperative venographic patterns of the postoperative recurrence and surgical incision placement of pediatric varicoceles. J Urol. 1990; 144:502–505

109. Zaonotz MR, Firli CF. Use of venography as an aid in varicocelectomy. J Urol. 1987;138:1041–1042

110. Hart RR, Rushton HG, Belman AB. Intraoperative spermatic venogra-phy during varicocele surgery in adolescents. J Urol. 1992;148: 1514 –1516

111. Reyes BL, Trerotola SO, Venbrux AC, et al. Percutaneous embolo-therapy of adolescent varicocele: results and long-term follow-up. J Vasc Interv Radiol. 1994;5:131–134

112. Goldstein M. Mini-incision microsurgical inguinal or subinguinal var-icocelectomy with delivery of the testis. Proceedings of the 44th An-nual Meeting of the Society for Pediatric Urology; 1994:1–5; May 14, 1994; San Francisco, CA

113. Atassi O, Kass EJ, Steinert BW. Testicular growth after successful varicocele correction in adolescents: comparison of artery sparing tech-niques with the Palomo procedure. J Urol. 1995;153:482– 483 114. Parrott TS, Hewatt L. Ligation of the testicular artery and vein in

adolescent varicocele. J Urol. 1994;152:791–793

FAT CATS

A quarter of dogs and cats in the US are too fat. Following a report from the Centers for Disease Control and Prevention in Atlanta which stated that 33% of men and 36% of women in the United States are overweight, veterinary researchers say their pets are little better.

Elizabeth Lund and her colleagues at the University of Minnesota at Minneap-olis-St Paul asked 50 vets in 30 states to rate how many of the cats and dogs they examined were too fat for bony structures, such as ribs, to be felt. About 25% of cats were overweight, and another 6% were obese. The same percentage of dogs were overweight and 5% obese.

New Scientist. March 29, 1997:13.

(12)

DOI: 10.1542/peds.100.1.112

1997;100;112

Pediatrics

Steven J. Skoog, Kenneth P. Roberts, Marc Goldstein and Jon L. Pryor

Patients?

The Adolescent Varicocele: What's New With an Old Problem in Young

Services

Updated Information &

http://pediatrics.aappublications.org/content/100/1/112

including high resolution figures, can be found at:

References

http://pediatrics.aappublications.org/content/100/1/112#BIBL

This article cites 106 articles, 3 of which you can access for free at:

Subspecialty Collections

http://www.aappublications.org/cgi/collection/gastroenterology_sub Gastroenterology

following collection(s):

This article, along with others on similar topics, appears in the

Permissions & Licensing

http://www.aappublications.org/site/misc/Permissions.xhtml

in its entirety can be found online at:

Information about reproducing this article in parts (figures, tables) or

Reprints

http://www.aappublications.org/site/misc/reprints.xhtml

(13)

DOI: 10.1542/peds.100.1.112

1997;100;112

Pediatrics

Steven J. Skoog, Kenneth P. Roberts, Marc Goldstein and Jon L. Pryor

Patients?

The Adolescent Varicocele: What's New With an Old Problem in Young

http://pediatrics.aappublications.org/content/100/1/112

located on the World Wide Web at:

The online version of this article, along with updated information and services, is

by the American Academy of Pediatrics. All rights reserved. Print ISSN: 1073-0397.

Figure

TABLE 1.Incidence of Varicocele in Children
Fig 2. Paracrine interactions in the testis. Pictured is a represen-tative sample of the known signaling molecules involved in cell-cell communication in the testis
TABLE 2.Treatment Options

References

Related documents

In summary and taking into account the resonance characteristics of the ACUREX plant, the main contribution of this paper, is to improve a gain schedul- ing (GS) predictive

Standardization of herbal raw drugs include passport data of raw plant drugs, botanical authentification, microscopic & molecular examination, identification of

Field experiments were conducted at Ebonyi State University Research Farm during 2009 and 2010 farming seasons to evaluate the effect of intercropping maize with

19% serve a county. Fourteen per cent of the centers provide service for adjoining states in addition to the states in which they are located; usually these adjoining states have

innovation in payment systems, in particular the infrastructure used to operate payment systems, in the interests of service-users 3.. to ensure that payment systems

The finding of the current study that marital status influenced teachers’ self-efficacy with the married having higher self-efficacy was similar to findings by Adio and Popola

Results suggest that the probability of under-educated employment is higher among low skilled recent migrants and that the over-education risk is higher among high skilled

It is much to be regretted that our diligent search for the upper part of this lintel was unsuccessful; for this inscription, judged by the style of its lettering,