obesitas mencegah varikokel

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ORI GI NAL ARTI CLE

The relationship between varicoceles and obesity in ayoung adult populationChih-Wei Tsao,* Chien-Yeh Hsu, Yu-Ching Chou, Sheng-Tang Wu,* Guang-Huan Sun,*

Dah-Shyong Yu,* Pao-Luo Fan,* Hong-I Chen,* Sun-Yran Chang* and Tai-Lung Cha**Division of Urology, Department of Surgery, Tri-Service General Hospital, Taipei, Graduate Institute of Medical Informatics,Taipei Medical University, Taipei, and School of Public Health, National Defence Medical Center, Taipei, Taiwan

Introduction

A varicocele is a dilatation of the scrotal portion of thepampiniform plexus to the internal spermatic venous sys-tem that drains the testis. Numerous studies have docu-mented an uneven detection rate of varicoceles in variousage groups in the general population. Population-basedstudies, largely school boy and adolescent physical exam-inations have led to estimates of varicocele prevalence inthe general population of 4.116.2%, respectively (Oster,1971; Steeno et al., 1976; Stavropoulos et al., 2002). The42% prevalence of varicoceles in the elderly population

was observed by Canales et al. (2005). The pathogenesisof varix formation, although somewhat unclear, isthought to be related to various factors resulting in anincreased pressure in the veins of the pampiniform plexusand its venous drainage.

Recently, Handel et al. (2006) and Nielsen et al. (2006)suggested that the degree of adiposity might have animportant role in the pathogenesis of varicocele, which isbased on the observation that varicoceles were less likely in obese men because of a decreased nutcracker effect orcompression to the left testicular vein with increasingbody mass index (BMI). As the above population groups

Keywords:body mass index, varicocele, visceral obesity,young adult

Correspondence:

Tai-Lung Cha, Division of Urology,Department of Surgery, Tri-Service GeneralHospital, No. 325, Section 2, Cheng-GungRoad, Neihu 114, Taipei, Taiwan.E-mail: [email protected]

Received 20 April 2008; revised 19 July 2008,20 August 2008; accepted 21 August 2008

doi:10.1111/j.1365-2605.2008.00926.x

Summary

To determine whether a relationship between obesity and varicocele occurrenceexists, the prevalence and severity of varicoceles related to obesity were investi-gated in a general population of young males. A total of 1050 young malesattending the Navy Recruit Training Center were evaluated from their physicalscreening examinations. All subjects underwent history taking and physicalexaminations to evaluate for the presence and severity of varicocele. Theanthropometric indexes including body mass index (BMI), waist circumference(WC) and waist-to-hip ratio (WHR) were recorded. All subjects were catego-rized by quartiles according to each anthropometric index. Means were com-pared with the Students t -test. Severity was compared by analysis of variancetesting and frequency was analysed using the chi-square method. Statistical sig-nicance was considered at p


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being composed of infertile patients, we were interestedin knowing the true relationship between varicoceles andobesity in a general population. The previous study of Chan et al. (2003) found that waist circumference (WC)was a stronger predictor of intra-abdominal adipose tissuemasses ( p < 0.05) than BMI, and there was no signicant

difference between WC and waist-to-hip ratio (WHR).The purpose of this study was to determine whether arelationship between varicoceles and obesity exists in a young population, and whether WC and WHR are corre-lated with the prevalence and severity of varicoceles.

Materials and methods

A single physician evaluated 1055 young military menattending the Navy Recruit Training Center. All subjectsunderwent history taking and physical examinations toevaluate the presence and severity of varicocele. Of theexaminees, ve males were excluded from the study because of incomplete records. The remaining 1050 maleshad complete data, including the anthropometric mea-sures of height, weight, WC, hip circumference (HC), ageand physical assessment for varicocele. All subjects under-went physical examination in a warm environment. Thepresence and grade of detection on physical examinationwere recorded. If bilateral varicoceles were present, thevaricoceles were graded in severity according to the larg-est varicocele. Varicoceles were categorized as grade I palpable only with Valsalva, grade II palpable withoutValsalva but not visible and grade III visible when theexaminee was standing.

Varicoceles were examined as presence or absence, andthe subjects of presence were divided into three groups by grade. BMI was calculated from the formula, weight inkilograms divided by height in metres squared. WC wasobtained from the mid-point between the iliac crest andcostal margin. HC was measured at the widest pointaround the greater trochanter. Both WC and HC weremeasured in centimetres. WHR was determined by theWC divided by the HC. Height, weight and all theseanthropometric indexes (including BMI, WC and WHR)were recorded according to the various varicocele groups(non-varicocele, grade I, grade II and grade III). Differ-ences in the above indexes among each various varicocelegroups were compared using the test of analysis of vari-ance (anova ). To illustrate the real association betweenvaricoceles and obesity, all subjects were categorized by quartiles according to each anthropometric index, analy-sing the severity and prevalence of varicoceles whileincreasing obesity. The frequencies of varicoceles in eachquartile category were compared by chi-square test. Anal- ysis of logistic regression was used to exhibit the trendbetween varicoceles and obesity in each anthropometric

index. To realize the more detailed association, weapplied the lineal regression model to predict the severity of varicocele with increasing adiposity in each anthropo-metric indicator. The method of logistic regression wasused to observe the variance of prevalence in each gradevaricocele group with increasing obesity of each anthro-

pometric index. All analyses were conducted using spssstatistical software (version 13.0; SPSS Inc, Chicago, IL,USA).

Results

All subjects were aged between 18 and 27 years and atotal of 490 (46.67%) subjects had varicoceles. The meanages of varicocele and non-varicocele population were19.79 and 19.86, respectively. There was rarely the clinicalsymptom of pain or discomfort combined with varicoce-les in this study. The means of BMI, WC and WHR with-out varicoceles were 23.99 3.82 kg m 2 , 83.20 9.97 cmand 0.85 0.05, respectively. These judged values of anthropometric indexes were greater than those withvaricoceles (22.02 3.18 kg m 2 , 79.19 9.01 cm and0.83 0.05; p < 0.001, Table 1). The mean value of eachanthropometric index had a signicantly statistical corre-lation ( anova test, all p < 0.001) with each grade varico-cele. The changes of height correlated positively withincreasing grade of varicoceles. ( p = 0.001, Table 2). Totest the obesity-inuence relationship, the severity andprevalence of varicoceles were examined by quartiles of these anthropometric indexes (BMI, WC and WHR). Wefound that the severity of varicoceles was inversely corre-

lated with increasing adiposity of all three anthropometricindexes. The applied lineal regression model showed apersistently and statistically reverse relationship betweenvaricocele severity and obesity (all p < 0.001, Table 3). Inother words, these results suggested that more obese menmay have less severity of varicocele.

Table 1 The comparison results of objects between with varicocelesand without varicoceles (Students t -test)

Variables

Men withoutvaricocelesmean (SD)n = 560

Men withvaricocelesmean (SD)n = 490

Age (years) 19.86 (2.05) 19.79 (1.84)Height (m) 1.70 (0.06) 1.72 (0.06)*Weight (kg) 69.69 (12.02) 65.01 (11.31)**BMI (kg m2 ) 23.99 (3.82) 22.02 (3.18)**WC (cm) 83.20 (9.97) 79.19 (9.01)**WHR 0.85 (0.05) 0.83 (0.05)**

BMI, body mass index; WC, waist circumference; WHR, waist-to-hipratio.* p < 0.005, ** p < 0.001.

Varicoceles and obesity C.-W. Tsao et al.

386 2008 The Authors

Journal compilation 2008 European Academy of Andrology International Journal of Andrology 32, 385390


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The prevalence of varicocele signicantly decreased withincreasing BMI from 61.98% in the lowest quartile of BMI to 25.75% in the highest quartile ( p < 0.001). Thesame correlation was observed among the other twoanthropometric indexes, WC and WHR, and both showedstatistical signicance (both p < 0.001). The relationshipbetween prevalence of each grade varicocele and obesity showed an inverse trend among each anthropometric

index (Fig. 1). To realize the detailed variance of the prev-alence of each grade varicocele with increasing adiposity according to the different anthropometric indicators, weapplied the logistic regression model to explain it. Theresults showed that, the odds ratio of grade II prevalencevariance kept within the range of 0.5800.807, the gradeIII of 0.5420.604, and both the variance of grade II andIII prevalence presented a statistically inverse relationshipwith increasing adiposity according to all three anthropo-metric indexes of BMI, WC and WHR ( p = 0.011, p < 0.001). On the other hand, although the variance of grade I prevalence showed a reverse trend with increasingobesity of three anthropometric indicators, only BMI wasstatistically signicant ( p = 0.047, Table 4).

Discussion

Smith (1957) was the rst to hypothesize that patientswith varicoceles were taller and heavier. The retrospectivestudy of Delaney et al. (2004) concluded that childrenwith varicoceles were signicantly taller and heavier, butdid not show signicant differences in BMI. Another

group, May et al. (2006) suggested that the children andadolescents aged 919 years with varicoceles were heavierand taller than an age-correlated normal population, buthad a distinctly lower BMI. Some speculated that agreater overall height was associated with an increasedhydrostatic pressure of the spermatic vein, which may inturn overwhelm the valve mechanisms in the veins,resulting in the development of varicocele (Shak & Bedeir, 1980). This speculation was in accordance withthe theory describing absence of or malfunctioningvenous valves as a potential cause of varicocele formation(Braedel et al., 1994). Our data support the concept of astatistically positive relationship between varicocele andheight. Increased pressure in the left internal spermaticvein may result from compression of the left renal veinbetween the aorta and the superior mesenteric artery, aphenomenon known as the nutcracker effect (Coolsaet,1980). The mechanism of nutcracker effect is not fully recognized. Retroperitoneal fat and the third segment of the duodenum are important in maintaining a wide

aorta-mesenteric angle (Stavros et al., 1994), and a nar-row aorta-mesenteric angle or an abnormal branching of the superior mesenteric artery from the aorta causes com-pression of left renal vein (LRV) (Arima et al., 1990; Sho-keir et al., 1994). Renal venography combined withmeasurement of the pressure gradient between the LRVand the inferior vena cava would be the most reliablemethod for demonstrating renal vein hypertension; how-ever, the diagnostic procedure would be more invasive.Besides peak velocity (PV) ratio of Doppler, sonography showed more sensitive and specic than LRV diameterratio of venography in detection of the nutcracker effect(Kim et al., 1996).

Among the adult population, recent reports of Handelet al. (2006) and Nielsen et al. (2006) emphasized thatless nutcracker effect or other biophysical effects of increased adiposity may play a role in prevention of varicoceles. They assert that fat around the left renal veinmay provide a cushion protecting against the nutcrackerphenomenon in the obese men. Because of not showingdirect inuence of adiposity on the nutcracker phenome-non, the other study of Shin et al. (2007) investigated an

Table 2 The mean values of anthropometricindexes according to each varicocele category Anthropometric

indexNon-varicocele(n = 560)

Grade I(n = 282)

Grade II(n = 137)

Grade III(n = 71) p-value a

H (m) 1.7037 1.7131 1.7165 1.7281 0.001BMI (kg m2 ) 23.9861 22.5924 21.3750 20.9680


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inverse relationship between BMI and the PV ratios of the left renal vein (aorta-mesenteric PV hilar PV, a diag-nostic criterion of nutcracker phenomenon) among themale patients; however, they did not examine the pres-ence of varicocele. From the above three studies, it wouldappear that the adiposity reducing the effect of the nut-cracker phenomenon may serve as a possible mechanismto prevent varicocele occurrence. However, there is nodirect evidence to show that the nutcracker effect corre-lates with the clinical presence of varicocele. Although therenal Doppler ultrasound is a non-invasive tool for detec-tion of nutcracker effect, real-time availability is limited.The visceral obesity has been proven to be involved inthe pathogenesis of cardiovascular disease, type 2 diabetesand dyslipidemia (Ginsberg, 2000; Kahn & Flier, 2000),and it seems to be more potentially harmful to endothe-lial function than obesity in general (Brook et al., 2001).According to our results, not only the general obesity assessed by BMI has statistically inverse relationship with

the severity of varicoceles, but also the visceral obesity assessed by WC and WHR were signicantly inversely correlated with varicoceles. Our results suggest thatincreased visceral obesity prevents the nutcracker effectand then results in less severity of varicoceles. As to theresult of general obesity correlating inversely with varico-celes, in accordance with the theory postulated by Dela-ney et al. (2004), which is that they thought increasedmass as it is related to BMI, was related to increasedmusculature. They noted that muscle tissue is denser thanadipose tissue, which accounts for clinical adolescentmales with varicoceles generally showing an athletic build.The effect of physical training on the natural history of varicocele has received little attention. One study by Rig-ano et al. (2004) reported a positive correlation betweenthe number of athletes with varicocele and the highestgrade of varicocele in the adolescents. Another study by Di Luigi et al. (2001) also found a high incidence of vari-cocele in adult athletes. As the subjects of our study

WC

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0.35Grade I

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Figure 1 The prevalence of each grade varicoceles in different quartile of body mass index (BMI), waist circumference (WC) and waist-to-hip ratio(WHR). The prevalence of grade I in each quartile of BMI: 28.5, 28.5, 30.9 and 19.8%; The prevalence of grade II in each quartile of BMI: 22.1,15.6, 9.8 and 4.9%; The prevalence of grade III in each quartile of BMI: 11.4, 9.5, 5.1 and 1.1%. The prevalence of grade I in each quartile ofWC: 27.0, 26.3, 29.2 and 25.0%; The prevalence of grade II in each quartile of WC: 19.7, 16.0, 11.4 and 6.0%; The prevalence of grade III ineach quartile of WC: 10.0, 11.5, 3.8 and 2.5%. The prevalence of grade I in each quartile of WHR: 24.5, 30.8, 28.5 and 23.5%; The prevalence

of grade II in each quartile of WHR: 18.3, 11.7, 12.4 and 10.0%; The prevalence of grade III in each quartile of WHR: 13.2, 6.4, 4.1 and 3.5%.





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received high-volume and intensive physical training, agreater prevalence of varicoceles was observed comparedwith other study groups.

Not only the prevalence but also the severity of varic-oceles showed signicantly inverse correlation with obes-ity. The grade III varicoceles appeared in the young menwith the least obesity according to all three anthropo-metric indexes. The explanation of Handel et al. (2006)supported our results, which excluded the possibility of obesity induced decreased detection of varicocelesbecause of difculty in palpation on physical examina-tion. As to the above theory, which would not expectthe prevalence of grade III varicoceles to decrease in

more obese men on account of being easily detected,and would expect the prevalence of grade I to be less inobese men because it is easily missed. On the contrary,our statistical results revealed the reverse conclusion.Therefore, difculty in detecting varicoceles because of obesity is less likely.

Few studies reported the correlation between varicoceleand sexual dysfunction. Kim & Choi (1992) detectedimprovement of the penile blood ow after correction of varicocele on scrotopenograms. Younes (2003) presentedthat the improvement of sexual activity in impotentpatients after receiving bilateral varicocelectomy was 5075%, including libido, morning erection, duration andpercentage of erection, sexual interest and frequency of erection per week. Some limitations of our retrospectivestudy such as the lack of associated data including semenquality and hormone variation are worth noting. Coordi-nating to clinical appearance of varicocele and the objec-tive measurement of Doppler PV ratio would support thepowerful evidence of nutcracker phenomenon. Furtherstudies including the following of the results of previousdata after a duration time should be designed.

Conclusion

We observed a signicantly inverse relationship betweenobesity and varicoceles among a large young populationattending training centre for a physical check-up. Theseverity and prevalence of varicoceles were not only nega-tively correlated with general obesity assessed by BMI, butalso negatively associated with visceral obesity assessed by WC and WHR. This result supported the possibility thatobesity results in a decreased nutcracker effect in whichthe adipose tissue may prevent compression of the renalvein.

References

Arima, M., Hosokawa, S., Ogino, T., Ihara, H., Terakawa, T. & Ikoma, F. (1990) Ultrasonographically demonstrated nut-cracker phenomenon: alternative to angiography. Interna-tional Urology and Nephrology 22, 36.

Braedel, H. U., Steffens, J., Ziegler, M., Polsky, M. S. & Platt,M. L. (1994) A possible ontogenic etiology for idiopathicleft varicocele. Journal of Urology 151, 6266.

Brook, R. D., Bard, R. L., Rubenre, M., Ridker, P. M. & Raj-agopalan, S. (2001) Usefulness of visceral obesity (waist hipratio) in predicting vascular endothelial function in healthy overweight adults. American Journal of Cardiology 88, 12641269.

Canales, B. K., Zapzalka, D. M., Ercole, C. J., Carey, P.,Haus, E., Aeppli, D. & Pryor, J. L. (2005) Prevalence andeffect of varicoceles in an elderly population. Urology 66,627631.

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Waist circumference, waist-to-hip ratio and body massindex as predictors of adipose tissue compartments in men.QJM 96, 441447.

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Delaney, D. P., Carr, M. C., Kolon, T. F., Snyder, H. M., 3rd& Zderic, S. A. (2004) The physical characteristics of youngmales with varicocele. BJU International 94, 624626.

Di Luigi, L., Gentile, V., Pigozzi, F., Giannetti, D. & Romanelli,F. (2001) Physical activity as a possible aggravating factorfor athletes with varicocele: impact on the semen prole.Human Reproduction 16, 11801184.

Ginsberg, H. N. (2000) Insulin resistance and cardiovasculardisease. Journal of Clinical Investigation 106, 453458.

Handel, L. N., Shetty, R. & Sigman, M. (2006) The relation-ship between varicoceles and obesity. Journal of Urology 176,21382140; discussion 2140.

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Kim, Y. C. & Choi, H. K. (1992) Clinical value of scrotopeno-gram for evaluating varicocele and erectile dysfunction.Urology 39, 150156.

Table 4 Logistic regression result of quartile prevalence variance ofthree anthropometric indexes according to each grade varicoceles

Anthropometricindex

Grade ofvaricoceles

O.R.(odds ratio) 95% C.I. p-value a

BMI I 0.884 0.7820.998 0.047II 0.580 0.4890.695


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Kim, S. H., Cho, S. W., Kim, H. D., Chung, J. W., Park, J. H.& Han, M. C. (1996) Nutcracker syndrome: diagnosis withdoppler us. Radiology 198, 9397.

May, M., Taymoorian, K., Beutner, S., Helke, C., Braun, K. P.,Lein, M., Roigas, J. & Hoschke, B. (2006) Body size andweight as predisposing factors in varicocele. Scandinavian Journal of Urology and Nephrology 40, 4548.

Nielsen, M. E., Zderic, S., Freedland, S. J. & Jarow, J. P. (2006)Insight on pathogenesis of varicoceles: relationship of vari-cocele and body mass index. Urology 68, 392396.

Oster, J. (1971) Varicocele in children and adolescents. Aninvestigation of the incidence among Danish school children.Scandinavian Journal of Urology and Nephrology 5, 2732.

Rigano, E., Santoro, G., Impellizzeri, P., Antonuccio, P.,Fugazzotto, D., Bitto, L. & Romeo, C. (2004) Varicocele andsport in the adolescent age. Preliminary report on the effectsof physical training. Journal of Endocrinological Investigation27, 130132.

Shak, A. & Bedeir, G. A. (1980) Venous tension patterns incord veins. I. In normal and varicocele individuals. Journal of Urology 123, 383385.

Shin, J. I., Park, J. M., Lee, J. S. & Kim, M. J. (2007) Effect of renal doppler ultrasound on the detection of nutcracker

syndrome in children with hematuria. European Journal of Pediatrics 166, 399404.

Shokeir, A. A., el-Diasty, T. A. & Ghoneim, M. A. (1994) Thenutcracker syndrome: new methods of diagnosis and treat-ment. British Journal of Urology 74, 139143.

Smith, S. M. (1957) Body size and weight in relation to varico-coele and hernia. Annals of Human Genetics 21, 304312.

Stavropoulos, N. E., Mihailidis, I., Hastazeris, K., Moisidou,R., Louka, G., Filiadis, I., Zouma, E., Danella, M. & Kalom-iris, P. (2002) Varicocele in schoolboys. Archives of Androlo- gy 48, 187192.

Stavros, A. T., Sickler, K. J. & Menter, R. R. (1994) Colorduplex sonography of the nutcracker syndrome (aortomes-enteric left renal vein compression). Journal of Ultrasound in Medicine 13, 569574.

Steeno, O., Knops, J., Declerck, L., Adimoelja, A. & van deVoorde, H. (1976) Prevention of fertility disorders by detection and treatment of varicocele at school and collegeage. Andrologia 8, 4753.

Younes, A. K. (2003) Improvement of sexual activity,pregnancy rate, and low plasma testosterone after bilateralvaricocelectomy in impotence and male infertility patients. Archives of Andrology 49, 219228.





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