Color Doppler ultrasound characteristics after subinguinal microscopic varicocelectomy
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- Marjorie Cox
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1 Oiginal aes Med Ultason 207, Vol 9, no, DOI: 052/mu-920 Colo Dole ultasound chaacteistics afte subinguinal micoscoic vaicocelectomy Muat Akand, Mustafa Kolay 2, Necat Islamoglu 2, Eme Altintas, Ozcan Kilic, Muat Gul, Haluk Kulaksizoglu 3, Mesut Sivi 2, Seda Goktas Selcuk Univesity, School of Medicine, Deatment of Uology, Konya, 2 Selcuk Univesity, School of Medicine, Deatment of Radiology, Konya, 3 Bilim Univesity, Sisli Floence Nightingale Hosital, Deatment of Uology, Istanbul, Tukey Abstact Aim: The esent study evaluated the effect of diffeences in the eak systolic velocity (PSV) and esistive index (RI) in the testicula atey (TA), casula atey (CA), and intatesticula atey (ITA) afte micoscoic subinguinal vaicocelectomy (MSV) on ostoeative ain and semen aametes Patients and methods: Scotal colo Dole ultasound (CDUS) measuements wee made in 33 atients (age 8-3 yeas) io to MSV and 3 and 6 months afte MSV Pain was ecoded using a visual analog scale and sem concentation was detemined to analyze the edictive value of the CDUS aametes egading sugical outcome Results: A significant decease in ain scoes was obseved in most atients at both follow-us The fist ostoeative CDUS evealed a significant incease in the TA-PSV () and a decease in the TA-RI (=0002) and CA- RI (=0006) The second ostoeative CDUS also evealed a significant incease in the TA-PSV and a decease in the TA-RI, and the PSV in the ITA and CA and RI in the ITA and CA wee significantly diffeent fom the values obtained e-oeatively and at the fist follow-u A negative coelation was found between the ain level and TA-PSV (=-0433, =002), wheeas sem concentation ositively coelated with both the TA-PSV and CA-PSV (=0534, =000 and =0455, =0008, esectively) Conclusions: The PSV and RI ae useful aametes fo detecting changes in testicula micohemodynamics afte MSV In addition, the TA-PSV and CA-PSV can be used to edict imovements in ain and sem concentation Keywods: vaicocele, ain, infetility, micoscoic vaicocelectomy, colo Dole ultasound Intoduction Received Acceted Med Ultason 207, Vol 9, No, Coesonding autho: Muat Akand, MD, FEBU Selçuk Ünivesitesi, Alaeddin Keykubat Kamüsü, Tı Fakültesi Hastanesi, E-Blok, Kat:, Üoloji Polikliniği, Kamüs- Selçuklu/Konya/Tükiye Phone: , Fax: dmuatakand@yahoocom Vaicocele is a hemodynamic imaiment with continuous blood eflux in the aminifom venous lexus The condition is chaacteized by abnomal dilatation and etogade blood flow in the affected veins [] and is esent in aoximately 5% of the geneal oulation The evalence is u to 35% in male oulation with imay infetility and can be as high as 75% in men with seconday infetility [2] Although the effects of vaicocele, including a educed volume of the affected testis, imaied sem oduction, educed fetility, and scotal ain, ae well established, the mechanism of testicula damage is still unclea [3] The most acceted athohysiology of vaicocele-associated infetility is inceased testicula temeatue seconday to venous eflux [4] Vaicocelectomy can be efomed by taditional oen sugey (high etoeitoneal, inguinal, o subinguinal), micoscoic sugey (inguinal o subinguinal), and laaoscoic aoach Regadless of diffeent modalities, changes in semen aametes have been demonstated Cayan et al [5] found an imovement in the quality of sematozoa in aoximately 70% of atients, wheeas anothe andomized contolled tial and a metaanalysis showed that vaicocelectomy imoves semen quality and educes seminal oxidative stess [6,7] In contast, Eves et al [8] demonstated that vaicocelectomy is not effective fo the teatment of male subfetility Futhemoe, Daitch et al [9] concluded that, although
2 60 Muat Akand et al Colo Dole ultasound chaacteistics afte subinguinal micoscoic vaicocelectomy vaicocelectomy did not imove semen aametes, it imoved the chance of egnancy and live bith ates in coules with male infetility that undewent intauteine insemination The testes ae sulied by thee majo ateies: the testicula atey (TA), the cemasteic atey, and the defeential atey The TA divides into two banches; the casula atey (CA) that continues on the suface of the testis and the intatesticula atey (ITA) that goes dee into the aenchyma of the testis [0] Scotal colo Dole ultasound (CDUS) has been established as an effective and accuate diagnostic tool fo examining the maco and micovasculaity of the testes, in which ateial flow velocities (eak systolic velocity [PSV] and end-diastolic velocity [EDV]) and esistance indices (eg, esistive index [RI] and ulsatility index [PI]) can be easily measued [0-2] In this study, we evaluated the effect of diffeences in the PSV and RI in the TA, CA, and ITA befoe and afte micoscoic subinguinal vaicocelectomy (MSV) on ostoeative ain and semen aametes Mateials and methods This study was eviewed and aoved by the Selcuk Univesity School of Medicine Ethics Committee (aoval 202/97) and efomed in accodance with the ethical standads in the 964 Declaation of Helsinki and its late amendments Witten infomed consent was obtained fom all atients The aim of the study was to evaluate whethe the PSV and/o RI can be used to edict sugical outcomes in egads to the e-oeative ain level and semen aametes Theefoe, the PSV and RI wee measued in thee diffeent levels of ateial suly (ie, the TA, CA, and ITA) befoe and afte MSV to identify coelations between these CDUS aametes and deceased ain and/ o imoved semen aametes Between June 202 and Mach 205, 82 men wee diagnosed with clinical vaicocele Fifty-nine of these atients undewent a left MSV and undewent a bilateal MSV in ou deatment The exclusion citeia fo this study wee bilateal vaicocele, any scotal athology othe than vaicocele, and a histoy of evious vaicocelectomy Thus, a total of 38 atients who had a left vaicocele esenting only with left scotal ain and infetility/abnomal semen aametes wee included in this osective study No comobidities, including hyetension, diabetes, o othe geneal diseases, wee esent in these atients The hysical examination was efomed in a wam oom and the Valsalva maneuve was efomed while the atient was standing uight [4] The degee of vaicocele was gaded clinically as gade I (vaicocele alable only duing Valsalva maneuve), gade II (vaicocele alable in standing osition), and gade III (vaicocele detectable by visual scutiny alone) [4] Pain was evaluated by a 0-oint visual analog scale (VAS) in which 0 was gaded as no ain and 0 as the wost ain in the atient s life Befoe the oeation, two seaate semen analyses wee efomed with an inteval of at least 2 weeks on samles obtained via mastubation afte 3-5 days of sexual abstinence The sem concentation and motility wee assessed using the Wold Health Oganization (WHO) 200 guidelines [3] Befoe sugey, all atients undewent CDUS efomed by the same adiologist (MK) using colo and Dulex ultasonogahy (Toshiba Alio 400, Tokyo, Jaan) with a linea 75 MHz tansduce in the suine osition Duing the examination, the diamete of the lagest vein in the aminifom lexus, the etogade flow in both the elaxed state and duing the Valsalva maneuve, and the PSV and RI of the TA, CA, and ITA wee measued (fig ) The esence of two o moe vaicose veins with a diamete of at least 3 mm and a etogade flow lasting moe than 2 seconds duing the Valsalva maneuve wee the diagnostic citeia defining a clinical vaicocele All of the atients undewent a left MSV unde sinal o geneal anesthesia by the same sugeon (MA) Using an oeating micoscoe (Cal Zeiss ) at 5-20x magnification, all intenal sematic veins wee identified, Fig CDUS image showing the measuement of the eak systolic velocity (PSV) and esistive index (RI) in a) at etesticula level: testicula atey (TA), b) at casula level: casula atey (CA), and c) at intatesticula level: intatesticula atey (ITA)
3 dissected, and ligated with 3-0 silk sutues and then divided while eseving vas defeens, vassal vessels, TA, and lymhatic vessels as much as ossible Patients wee examined caefully fo an extenal sematic vein; if esent it was also ligated and divided All atients wee dischaged the day afte sugey without any ei-oeative comlications All atients wee scheduled fo a follow-u at 3 and 6 months to evaluate ain and to efom a semen analysis and scotal CDUS Comlications, such as hydocele and testicula atohy, wee also examined duing the follow-u Patients wee classified into fou gous accoding to thei VAS scoes: no (0), mild (-4), modeate (5-6), and sevee (7-0) ain [4] An at least 3-oint decease in the VAS scoe o no ain at all at 6 months was defined as successful ain imovement Patients wee also consideed to have had a successful o failed oeation based on sem concentation ( 5 million/ml and <5 million/ ml, esectively) [3] Statistical analysis The nomality of the distibutions was evaluated using the Shaio-Wilk test Wilcoxon, aied t, Mann Whitney U, and Fiedman tests wee used to test the diffeences between gou numbes and aied o unaied gous as aoiate The esults wee exessed as mean ± standad deviation, median (min max), o numbe (fequency) The Seaman ho coelation coefficient was used to indicate elationshis between vaiables The significance level (α) was 005 and a twotailed <005 was consideed significant All statistical analyses wee efomed using SPSS 50 (SPSS Inc, Chicago, IL, USA) Results Med Ultason 207; 9(): Postoeative data wee missing fo 2 atients at the fist follow-u and 3 atients at the second follow-u; theefoe, 33 atients wee evaluated in the final analysis The mean age was 255 ± 45 yeas (median 26 yeas, ange 8-3 yeas) Nineteen atients (576%) had gade II and 4 atients (424%) gade III vaicocele Duing MSV, the median numbe of ligated veins was 9 (ange 4-2), and 20 atients (606%) had an extenal sematic vein The mean duation of MSV was 724 ± 46 min (ange 50-8 min) No atient had hydocele o testicula atohy duing the follow-u Pe-oeative and ostoeative ain scoes, sem aametes, vein diametes, and the PSV and RI of the TA, CA, and ITA ae eoted in Table I A significant decease in ain scoes was obseved in the majoity of atients at both follow-us Only fou atients did not have imoved ain scoes Based on the sem concentations at 6 months, 2 atients (636%) had a successful oeation Scotal CDUS at 3 months evealed a significant incease in the TA-PSV and a significant decease in the TA-RI and CA-RI Howeve, CDUS at 6 months evealed a significant incease in the TA-PSV and a decease in the TA-RI comaed to the e-oeative value Howeve, the PSV of the ITA and CA significantly inceased and the RI of the ITA and CA significantly deceased with esect to both the e-oeative and 3-month values At the fist follow-u, a significant ositive coelation was obseved between the TA-PSV and ITA-PSV (=0358, =004), TA-PSV and CA-PSV (=0469, =0006), and ITA-PSV and CA-PSV (=046, =0007) 6 Table I Peoeative and ostoeative (at 3 and 6 months) ain scoes, sem aametes, vein diametes, and scotal CDUS aametes of the atients (n=33) Paametes Peoeative Postoeative- (3 d month) Postoeative-2 (6 th month) value Pain (VAS scoe) 60 ± 9 22 ± 4* 6 ± 4* Concentation (million/ml) 85 ± ± 337* 362 ± 338* $ Motility (%) 543 ± ± 97* 705 ± 20* Vein Diamete (mm) 36 ± ± 09* 27 ± 08* # TA PSV (cm/sec) 94 ± 9 4 ± 38** 5 ± 35 RI 069 ± ± 0* 06 ± 0* ITA PSV (cm/sec) 69 ± ± ± RI 057 ± ± ± CA PSV (cm/sec) 82 ± 2 89 ± ± 27* RI 063 ± ± ± 009 Data ae given in mean ± SD CDUS: Colo Dole ultasound, SD: Standad deviation, VAS: Visual analog scale, TA: Testicula atey, ITA: Intatesticula atey, CA: Casula atey, PSV: Peak systolic velocity, RI: Resistive index *, comaison with eoeative, Wilcoxon test; ** =0002, comaison with eoeative, aied-t test; =0006, comaison with eoeative, aied-t test;, comaison with eoeative, aied-t test; =0007, comaison with eoeative, Wilcoxon test; =0003, comaison with ostoeative-, Wilcoxon test; $, comaison with ostoeative-, Wilcoxon test; # =0024, comaison with ostoeative-, Wilcoxon test; =004, comaison with ostoeative-, Wilcoxon test; =0006, comaison with ostoeative-, Wilcoxon test; =0003, comaison with ostoeative-, aied-t test; =007, comaison with ostoeative-, aied-t test
4 62 Muat Akand et al Colo Dole ultasound chaacteistics afte subinguinal micoscoic vaicocelectomy A negative coelation was found between the PSV and RI of the TA (=-049, =0004), ITA (=-067, ), and CA (=-064, ) Although the TA-RI did not coelate with any of these aametes, the ITA-RI ositively coelated with the CA-RI (=0597, ) The negative coelation between the PSV and RI of the TA and ITA continued to exist between the fist and second follow-u (=-0446, =0009 and =-0354, =0043, esectively) The coelations between the 6-month values and e-oeative values ovided much moe infomation about the esults of the oeation A negative coelation was found between the ain level and TA-PSV (=-0433, =002), wheeas sem concentation ositively coelated with both the TA-PSV (=0534, =000) and CA- PSV (=0455, =0008) The negative coelation found between the sem concentation and ain (=-0476, =0005) might indicate that the oeation was successful in tems of both ain elief and sem concentation All othe coelations between CDUS aametes, excet between the TA-RI and ITA-PSV, wee significant (Table II) The incease in the PSV ofn the TA, ITA, and CA and the decease in the RI of the TA, ITA, and CA wee still esent at 6 months Theefoe, the ositive coelations between these values and the negative coelation between the PSV and RI in these thee ateies wee maintained No diffeences wee obseved in the CDUS aametes, excet the TA-RI, between atients with o without successful ain elief, (062 vs 050, esectively; =0047) As the -value was vey close to the cut-off, this elationshi can be ignoed (Table III) When the atients with a successful o failed oeation in tems of sem concentation wee evaluated, significant diffeences wee obseved only in the PSV of the ITA and CA at the fist follow-u, and in the PSV of the TA and CA at the second follow-u (Table IV) Table II Coelations within CDUS aametes at 6 months afte sugey TA-PSV TA-RI ITA-PSV ITA-RI CA-PSV CA-RI TA-PSV TA-RI ITA-PSV ITA-RI CA-PSV CA-RI CDUS: Colo Dole ultasound, TA: Testicula atey, TA: Intatesticula atey, CA: Casula atey, PSV: Peak systolic velocity, RI: Resistive index Table III Peoeative and ostoeative (at 3 and 6 months) scotal CDUS aametes of the atients with o without success in ain elief (n=33) Peoeative Postoeative- (at 3 months) Postoeative-2 (at 6 months) Paametes No (n=4) (n=29) value No (n=4) (n=29) value No (n=4) (n=29) value TA PSV 9 ± ± ± 45 9 ± ± 55 8 ± RI 058 ± ± ± ± ± ± ITA PSV 80 ± ± ± 4 73 ± ± 4 78 ± RI 06 ± ± ± ± ± ± CA PSV 69 ± ± ± 8 9 ± ± ± RI 062 ± ± ± ± ± ± CDUS: Colo Dole ultasound, TA: Testicula atey, ITA: Intatesticula atey, CA: Casula atey, PSV: Peak systolic velocity, RI: Resistive index All values ae given as mean ± SD
5 Med Ultason 207; 9(): Table IV Peoeative and ostoeative (at 3 and 6 months) scotal CDUS aametes of the atients with o without success in sem concentation (n=33) Peoeative Postoeative- (at 3 months) Postoeative-2 (at 6 months) Paametes No (n=2) (n=2) value No (n=2) (n=2) value No (n=2) (n=2) value TA PSV 9 ± 7 95 ± ± 52 9 ± ± ± RI 069 ± ± ± ± ± ± ITA PSV 66 ± 5 7 ± ± 7 80 ± ± 2 83 ± RI 055 ± ± ± ± ± ± CA PSV 74 ± 8 87 ± ± 7 00 ± ± ± 22 RI 06 ± ± ± ± ± ± CDUS: Colo Dole ultasound, TA: Testicula atey, ITA: Intatesticula atey, CA: Casula atey, PSV: Peak systolic velocity, RI: Resistive index All values ae given as mean ± SD 63 Discussions Vaicocele is a common entity in daily uological actice, esecially in infetile men Though the disode may be comletely asymtomatic, scotal ain and/ o fetility oblems can occu CDUS is a useful and non-invasive tool fo the diagnosis and follow-u of vaicocele and has a sensitivity of 83-95% [5,6] The technique hels measue the testicula dimensions, the diametes of dilated veins, the etogade flow, and the ateial flow aametes, such as the PSV, EDV, RI, and PI The effects of vaicocelectomy on semen aametes and on egnancy ates ae well studied, but elatively little is known about the changes in the micovasculatue of the testicles afte sugey [5-9] A few yeas ago, diffeent eseach gous evaluated the micohemodynamics of the testes afte vaicocelectomy and eoted diffeent esults [7,8] The changes in the micohemodynamics of the testes ecently became a hot toic yet again, with some authos tying to find a coelation between CDUS aametes and sugical outcomes We aimed to identify a CDUS aamete that can hel edict ain eduction and/o imoved semen aametes Tanivedi et al obseved no change in the maximal and minimal flow ates o the RI afte micosugical and high ligation vaicocelectomy, concluding that no significant imaiment of testicula ciculation occued afte sugey [7] Unsal et al found a significant diffeence in the RI and PI of the CA in vaicocele atients comaed to a contol gou [8] Keeing in mind that thee was a small numbe of cases in thei study, the authos ointed out that these indices may be an indicato of imaied testicula micociculation Late, Balci et al wee the fist to show a significant decease in the mean intatesticula RI with an imovement in semen aametes and concluded that a decease in the RI suggests an imovement in the testicula blood suly [] Howeve, they did not find a coelation between the diffeence in the RI and an imovement in the total motile sem count, obably because of the small numbe of atients Tahan et al investigated the long-tem effects of inguinal MVS on blood flow and semen aametes [2] The PSV and EDV wee inceased in the left TA, and the RI and PI of the left CA and ITA wee deceased, but the authos did not obseve any change in these aametes in the ight ateies They also found a significant coelation between the semen analysis and the PSV, RI, and PI of the left CA [2] With a significant coelation between imoved testicula hemodynamics and semen aametes, the authos suggested that testicula blood flow aametes could be used in the ostoeative follow-u of atients with vaicocele Two vey ecent studies coelated imovements in testicula blood flow aametes and semen analysis Zhang et al showed that the PSV, RI, and PI of the left CA and ITA deceased significantly afte laaoscoic vaicocelectomy and MSV, but no significant diffeence was noted in the EDV [9] Seaately evaluating these diffeences fo the two aoaches, the authos found that MSV ovided a bette and ealie imovement in these aametes They also concluded that the RI and PI of the ITA and CA ae two imotant indices fo edicting the ognosis afte vaicocelectomy Ene et al evaluated the ateial flow, esistance, and sem aametes befoe and 3 months afte subinguinal vaicocelectomy [20] A significant incease in the PSV and EDV with a significant decease in the PI and RI of the left CA coelated with a significant imovement in the sem concentation, ogessive motility, and mohology at 3 months Howeve, they wee not able to show a significant diffeence in the CDUS aametes of atients with imoved semen aametes comaed to those without imoved semen aametes, which they easoned was due to the small numbe of atients in thei study We obseved a significant incease in the PSV of the TA, ITA, and CA, as well as a significant decease in the
6 64 Muat Akand et al Colo Dole ultasound chaacteistics afte subinguinal micoscoic vaicocelectomy RI of the same ateies The changes in the PSV and RI of the TA wee moe ominent, which may be due to the wide diamete of this atey comaed to the othe two Assessing the PSV and EDV in the CA and ITA is geneally moe difficult because these ateies ae smalle and moe totuous and have a lowe flow velocity Moeove, evaluation of these blood flow aametes with CDUS deends on the angle of insonation and the vessel diametes, wheeas the PI and RI do not deend on these factos [2] Zhang et al evaluated only the CA and ITA 6 months afte sugey, wheeas we assessed the PSV and RI of the TA, CA, and ITA at 3 and 6 months afte sugey [9] Although the significant decease in the RI of the CA and ITA was simila to thei findings, we also obseved an incease in the PSV in these ateies Thus, ou esults ae atly simila to those of Ene et al [20], though they only assessed the CA at 3 months Tanivedi et al assessed the RI at 7 days afte vaicocelectomy and failed to show any change [7] The authos citicized themselves, as vey ealy ostoeative evaluation may not ovide accuate infomation about testicula hemodynamics Simila to Tahan et al [2], we also think that late assessment of these aametes would ovide moe infomation about the micohemodynamics of the testes and the success of the oeation because it may take seveal months fo the edema and inflammation in the oeative field to ecove We think that a geate numbe of significant coelations between the e-oeative and second ostoeative values oves this hyothesis Ou esults show that imoved ain levels, sem aametes, and CDUS aametes continue u to 6 months afte sugey This imovement may likely continue afte 6 months The PSV in the thee ateies continued to incease as the RI values deceased, which shows the ongoing changes in the micohemodynamics of the testes The TA-PSV and CA-PSV seem to have the otential fo use in edicting imovements in sem concentation, wheeas the TA-PSV can be used fo ain elief When the diffeences in CDUS aametes between atients with successful and failed sugey in tems of both ain and sem concentation wee consideed, a few aametes wee found to have significant edictive value The TA-PSV was significant when all atients wee evaluated, but the TA-RI seemed to have value fo edicting an imovement in ain in the subgou assessment, though it was not significant and is not enough to conclude a fim coelation The inclusion of elatively few atients may have had an effect on this esult When consideing successful and failed sugey based on the sem concentation, the PSV of the ITA and CA at 3 months and the PSV of the TA and CA at 6 months had the otential to edict the outcome The CA-PSV was significant at both follow-us Taken togethe, the esults indicate that the CA-PSV can be used to diffeentiate atients with successful sugeies based on sem concentation This study has some limitations Fist, a elatively small numbe of atients was enolled in the study and 5 atients wee lost to follow-u, which may have affected the statistical analysis Second, sem mohology was not evaluated due to missing data Thid, only the PSV and RI wee measued on scotal CDUS Including the EDV and PI would have been beneficial Nonetheless, this study has some imotant stengths Relatively young and healthy atients wee evaluated, which made the study cohot quite homogenous In addition, all atients wee oeated on by the same sugeon using a micosugical technique, and all scotal CDUSs wee efomed by the same adiologist and all semiogams in the same laboatoy Moeove, two ostoeative follow-us wee efomed, which made the esults moe consistent and eliable Conclusion Even with limited aametes, scotal CDUS is a useful tool fo detecting changes in the micohemodynamics of the testes afte MSV and edicting the sugical outcome The TA-PSV and CA-PSV can be used to edict imovements in ain and sem concentation Posective contolled studies in lage cohots ae needed to undestand whethe the coelation of blood flow and esistance aametes with sugical outcomes is esistent in the long-tem ostoeative eiod and whethe these aametes can be used outinely in clinical actice Conflict of inteest: none Acknowledgments: We would like to thank M M Boa Edogdu fo his valuable hel with the statistical analysis This oject was funded by the Selcuk Univesity Coodinatoshi of Scientific Reseach Pojects (BAP) (gant numbe ) Refeences Cimado M, Castagnetti M, Gattuccio I, Pensabene M, Segio M, De Gazia E The hemodynamic aoach to evaluating adolescent vaicocele Nat Rev Uol 202;9: Goldstein M Sugical management of male infetility In: Wein A, Kavoussi LR, Novick AC, Patin AW, Petes CA Editos Cambell-Walsh Uology Philadelhia, PA: Elsevie Saundes; 202:
7 3 Schaue I, Madesbache S, Jost R, Hubne WA, Imhof M The imact of vaicocelectomy on sem aametes: a meta-analysis J Uol 202;87: Vanlangenhove P, Dhondt E, Eveaet K, Defeyne L Pathohysiology, diagnosis and teatment of vaicoceles: a eview Mineva Uol Nefol 204;66: Cayan S, Shavakhaov S, Kadioglu A Teatment of alable vaicocele in infetile men: a meta-analysis to define the best technique J Andol 2009;30: Abdel-Meguid TA, Al-Sayyad A, Tayib A, Fasi HM Does vaicocele eai imove male infetility? An evidencebased esective fom a andomized, contolled tial Eu Uol 20;59: Baazeem A, Belzile E, Ciami A, et al Vaicocele and male facto infetility teatment: a new meta-analysis and eview of the ole of vaicocele Eu Uol 20;60: Eves JL, Collins JA Assessment of efficacy of vaicocele eai fo male subfetility: a systematic eview Lancet 2003;36: Daitch JA, Bedaiwy MA, Pasqualotto EB, et al Vaicocelectomy imoves intauteine insemination success ates in men with vaicocele J Uol 200;65: Pinggea GM, Mittebege M, Batsch G, et al Assessment of the intatesticula esistive index by colou Dole ultasonogahy measuements as a edicto of sematogenesis BJU Int 2008;0: Balci A, Kaazinci S, Gou S, Sumbas H, Egilmez E, Inandi T Long-tem effect of vaicocele eai on intatesticula ateial esistance index J Clin Ultasound 2008;36: Tahan S, Uce O, Sahin MO, Gumus B Long-tem effect of micosugical vaicocelectomy on testicula blood flow J Andol 20;32:33-39 Med Ultason 207; 9(): Cooe TG, Noonan E, von Eckadstein S, et al Wold Health Oganization efeence values fo human semen chaacteistics Hum Reod Udate 200;6: Jensen MP, Chen C, Bugge AM Inteetation of visual analog scale atings and change scoes: a eanalysis of two clinical tials of ostoeative ain J Pain 2003;4: Schuich M, Aigne F, Fausche F, Pallwein L The ole of ultasound in assessment of male fetility Eu J Obstet Gynecol Reod Biol 2009;4(sul ):S92-S98 6 El-Hagga S, Nassef S, Gadalla A, Latif A, Mostafa T Ultasonogahic aametes of the sematic veins at the inguinal and scotal levels in vaicocele diagnosis and ostoeative eai Andologia 202;44: Tanıvedi O, Mioglu C, Hoasanlı K, Altay B, Caliskan KC, Gumus E Testicula blood flow measuements and mean esistive index values afte micosugical and high ligation vaicocelectomy Uology 2006;67: Unsal A, Tugut AT, Taskin F, Kosa U, Kaaman CZ Resistance and ulsality index incease in casula banches of testicula atey: indicato of imaied testicula micociculation in vaicocele? J Clin Ultasound 2007;35: Zhang M, Du L, Liu Z, Qi H, Chu Q The effects of vaicocelectomy on testicula ateial blood flow: laaoscoic sugey vesus micosugey Uol J 204;: Ene K, Ucgul YE, Okulu E, et al Comaison of ateial blood suly to the testicles in the eoeative and ealy ostoeative eiod in atients undegoing subinguinal vaicocelectomy Scand J Uol 205;49: Machesini AC, Magio FA, Beezowski AT, Neto OB, Nogueia AA, Candido dos Reis FJ A citical analysis of Dole velocimety in the diffeential diagnosis of malignant and benign ovaian masses J Womens Health (Lachmt) 2008;7:
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