The risk of TESE-induced hypogonadism: a systematic review and meta-analysis.

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Insulin 7237 depressed mood, dysthymiaDecreased energy/fatigue/sleep disturbances/increased sleepinessMetabolic syndrome Insulin resistance and type-2 diabetes mellitusDiminished cognitive function/poor concentration and memory,
testosterone 742 procedure is not without complications and haematoma, devascularization, inflammation and a decrease in testosterone levels have been described as such. The prevalence and duration of hypogonadism and associated symptoms
testosterone 1013 systematically.OBJECTIVE AND RATIONALEIn this systematic review we addressed the following research questions: Are serum testosterone levels decreased after TESE and, if so, do these levels recover over time? What is the prevalence of
testosterone 1205 is the prevalence of symptoms and signs related to hypogonadism after TESE and are they related to testosterone levels?SEARCH METHODSWe searched the databases Pubmed and Embase from 1 January 1993 to 26 June 2017.
testosterone 1534 included all studies that reported on TESE, regardless of the specific technique used, that measured testosterone and/or LH, and/or had information on signs or symptoms related to hypogonadism as defined by hypogonadism
testosterone 1947 Non-randomized Studies—of Interventions tool.OUTCOMESWe identified 15 studies reporting on total testosterone levels of which five studies also reported on testicular volume and one study on erectile dysfunction.
testosterone 2170 with Klinefelter syndrome and men with non-obstructive azoospermia had the strongest decrease in total testosterone levels 6 months after TESE, with a mean decrease of 4.1 and 2.7 nmol/l, respectively, which recovered
testosterone 2411 26 and 18 months after TESE, respectively. At 6 months after TESE, some studies reported serum total testosterone concentrations below a cut-off value of 12 nmol/l, where symptoms and signs related to hypogonadism
testosterone 2624 may appear. Furthermore, an increased prevalence of erectile dysfunction related to decreased total testosterone levels 6 months after TESE was reported. Also, in some men a decrease in testicular volume was reported.
testosterone 2793 men a decrease in testicular volume was reported. However, it is not clear if this is related to low testosterone levels.WIDER IMPLICATIONSThe transient, but statistically significant, decrease in total testosterone
testosterone 2895 testosterone levels.WIDER IMPLICATIONSThe transient, but statistically significant, decrease in total testosterone levels indicates that men are at risk of developing a temporary hypogonadism after TESE, but there is
testosterone 3118 insufficient evidence for whether patients actually experience clinical symptoms in case of decreased serum testosterone levels. To be able to properly counsel TESE patients, more large-scale monitoring on signs and symptoms
testosterone 3272 TESE patients, more large-scale monitoring on signs and symptoms of hypogonadism, in combination with testosterone measurements, needs to be performed in men undergoing TESE.IntroductionTesticular sperm extraction (TESE)
testosterone 5539 described, eventually leading to scars and calcification ([31]; [15]). Furthermore, a decrease in serum testosterone levels after a TESE procedure has been described ([15]; [33]). Decreased testosterone levels can subsequently
testosterone 5625 decrease in serum testosterone levels after a TESE procedure has been described ([15]; [33]). Decreased testosterone levels can subsequently lead to hypogonadism. Symptoms of hypogonadism have been described to occur
testosterone 5760 subsequently lead to hypogonadism. Symptoms of hypogonadism have been described to occur more often when total testosterone levels are below a threshold of 12 nmol/l, and the lower the total testosterone values, the more frequent
testosterone 5840 more often when total testosterone levels are below a threshold of 12 nmol/l, and the lower the total testosterone values, the more frequent the symptoms of hypogonadism will be present ([4]; [14]; [44]).According to
testosterone 6450 manifestations are not specific for hypogonadism, the diagnosis should always be confirmed by measuring serum testosterone levels ([3]; [14]). Table ISigns and symptoms associated with androgen deficiency in men.Small testes/shrinking
testosterone 7763 after TESE. We therefore systematically reviewed the literature and included all studies that measured testosterone levels, LH levels and/or signs and symptoms related to hypogonadism before and after TESE. In this systematic
testosterone 7956 after TESE. In this systematic review we addressed the following research questions: Are serum total testosterone levels decreased after TESE and, if so, do these levels recover over time? What is the prevalence of
testosterone 8154 the prevalence of symptoms and signs related to hypogonadism after TESE and are they related to total testosterone levels?MethodsThis review is reported according to the PRISMA statement ([39]). Prior to the search,
testosterone 9482 study-design. There were no restrictions in TESE techniques. We included all studies which measured testosterone , LH, or signs or symptoms related to hypogonadism (Table I), defined according to international hypogonadism
testosterone 9935 excluded studies that included prepubertal boys because of the difference in baseline characteristics and testosterone and LH levels compared to adult men.Data extractionOne author (J.E.) extracted data from the included
testosterone 11010 measurements of outcomes and selection of the reported results.Data analysesTo study the effect of TESE on testosterone levels over time we used the mean testosterone levels from individual studies to perform meta-regression
testosterone 11057 results.Data analysesTo study the effect of TESE on testosterone levels over time we used the mean testosterone levels from individual studies to perform meta-regression analyses using STATA 14.2 software (StataCorp,
testosterone 12806 testicular sperm extraction.Study characteristicsAll 15 included studies reported on serum levels of total testosterone before and after TESE. Nine studies also reported serum LH levels and six studies reported on symptoms
testosterone 13205 men and the study with the largest number of patients included 435 men, although they only reported testosterone levels before and after TESE from 142 men. The age of the men varied between 25 and 61 years. In all
testosterone 17473 samples were taken for hormone levels (n = 4), or studies that did not report cut-off values on low total testosterone (n = 1). In studies that reported a different follow-up time per man we also assessed the risk of bias
testosterone 17979 from the literature review.Testosterone levels after TESEFrom the 15 studies that measured serum total testosterone levels before and after TESE, one study only reported the testosterone levels of the men with new-onset
testosterone 18050 studies that measured serum total testosterone levels before and after TESE, one study only reported the testosterone levels of the men with new-onset of ED after TESE. In these men, serum total testosterone levels were
testosterone 18140 reported the testosterone levels of the men with new-onset of ED after TESE. In these men, serum total testosterone levels were significantly decreased after TESE ([1]). Another study reported a decrease of serum testosterone
testosterone 18250 testosterone levels were significantly decreased after TESE ([1]). Another study reported a decrease of serum testosterone levels 3–6 months after TESE, and a recovery of these levels after 18 months in both microdissection
testosterone 18483 TESE, but did not report SDs ([27]). We did not include these two studies in our meta-analyses.Mean testosterone levels after TESETwelve studies compared mean total testosterone levels before and after TESE (Table
testosterone 18548 studies in our meta-analyses.Mean testosterone levels after TESETwelve studies compared mean total testosterone levels before and after TESE (Table III). Meta-regression analysis showed a significant decrease in
testosterone 18667 before and after TESE (Table III). Meta-regression analysis showed a significant decrease in total testosterone levels at 3, 6, 9 and 12 months after TESE compared to before, which recovered to normal values again
testosterone 18838 before, which recovered to normal values again at 18 months (Fig. 3A). There was a lot of variation in testosterone levels between studies before TESE. To reduce this heterogeneity we analysed two patient groups separately,
testosterone 19156 possible to identify separate data for men with OA. Table IIICharacteristics of studies that measured testosterone levels after TESE.First author (year of publication)Technique testosterone measurementTime of blood
testosterone 19231 of studies that measured testosterone levels after TESE.First author (year of publication)Technique testosterone measurementTime of blood samplesTime after TESE measuredThreshold used for low testosterone levelsNumber
testosterone 19323 publication)Technique testosterone measurementTime of blood samplesTime after TESE measuredThreshold used for low testosterone levelsNumber participants with data availableType of outcomeManning (1998)Not described08.00 AM6 and
testosterone 19484 availableType of outcomeManning (1998)Not described08.00 AM6 and 12 monthsNot described15 (12 months n = 8)Mean testosterone levels and prevalence low testosteroneWestlander (2001)Not describedNot described3 and 6 monthsNot described35Mean
testosterone 19523 described08.00 AM6 and 12 monthsNot described15 (12 months n = 8)Mean testosterone levels and prevalence low testosterone Westlander (2001)Not describedNot described3 and 6 monthsNot described35Mean testosterone levelsSteele
testosterone 19612 prevalence low testosteroneWestlander (2001)Not describedNot described3 and 6 monthsNot described35Mean testosterone levelsSteele (2001)Radioimmunoassay by Coat-A-Count technology.Not described4 weeks≤12 nmol/l8Mean
testosterone 19726 levelsSteele (2001)Radioimmunoassay by Coat-A-Count technology.Not described4 weeks≤12 nmol/l8Mean testosterone levels and individual testosterone levelsOkada (2002)*RadioimmunoassayNot described6 monthsSignificant
testosterone 19761 by Coat-A-Count technology.Not described4 weeks≤12 nmol/l8Mean testosterone levels and individual testosterone levelsOkada (2002)*RadioimmunoassayNot described6 monthsSignificant decrease was defined as: When testosterone
testosterone 19872 testosterone levelsOkada (2002)*RadioimmunoassayNot described6 monthsSignificant decrease was defined as: When testosterone level was normal before TESE and after TESE <1.4 ng/ml or a decrease >1 ng/ml for men with hypogonadism
testosterone 20088 before TESEConventional TESE: n = 40microdissection TESE: n = 80Prevalence significant decrease in testosterone levelsSchill (2003)Competitive enzyme immunoassay, part of an automatic measuring apparatus, SR108.00–10.00
testosterone 20292 apparatus, SR108.00–10.00 AMAverage 18 months (4 to 32)<12 nmol/lBefore TESE: n = 26after TESE: n = 39Mean testosterone levels and prevalence low testosteroneKomori (2004)Not described09.00–11.00 AM1, 6 and 12 monthsNot
testosterone 20331 (4 to 32)<12 nmol/lBefore TESE: n = 26after TESE: n = 39Mean testosterone levels and prevalence low testosterone Komori (2004)Not described09.00–11.00 AM1, 6 and 12 monthsNot describedMultiple TESE: n = 13microdissection
testosterone 20476 described09.00–11.00 AM1, 6 and 12 monthsNot describedMultiple TESE: n = 13microdissection TESE: n = 12Mean total testosterone levelsRamasamy (2005)*Not described07.00–10.00 AM3, 6, 12 and 18 monthsNot described3–6 months:
testosterone 20635 described07.00–10.00 AM3, 6, 12 and 18 monthsNot described3–6 months: n = 14212 months: n = 8818 months: n = 53Mean testosterone levelsEveraert (2006)Radioimmunoassay08.00–10.00 AM2.4 years ± 1.1 years<280 ng/dlBefore TESE: n
testosterone 20776 (2006)Radioimmunoassay08.00–10.00 AM2.4 years ± 1.1 years<280 ng/dlBefore TESE: n = 45 after TESE: n = 31Mean testosterone levels and number of men with de novo androgen deficiencyTakada (2008)Solid-phase [125]I radioimmunoassay
testosterone 20990 radioimmunoassay kit Coat-A-Count08.00–11.00 AM3, 6, and 12 monthsNot describedKF: n = 9NOA: n = 60Mean total testosterone levelsIshikawa (2009)Not described09.00–10:00 AM1, 3, 6, 9, 12, and 18 monthsNot describedKF: n =
testosterone 21128 described09.00–10:00 AM1, 3, 6, 9, 12, and 18 monthsNot describedKF: n = 40NOA: n = 100Changes in testosterone levels relative to baseline testosterone levelsAkbal (2010)*Not described09.00–11.00 AM6 monthsNot
testosterone 21169 and 18 monthsNot describedKF: n = 40NOA: n = 100Changes in testosterone levels relative to baseline testosterone levelsAkbal (2010)*Not described09.00–11.00 AM6 monthsNot describedData of men with new-onsetED: n
testosterone 21298 (2010)*Not described09.00–11.00 AM6 monthsNot describedData of men with new-onsetED: n = 13Mean total testosterone levelsOzturk (2011)Not described09.00–11.00 AM3 and 12 monthsNot described37Mean total testosterone
testosterone 21400 testosterone levelsOzturk (2011)Not described09.00–11.00 AM3 and 12 monthsNot described37Mean total testosterone levelsBobjer (2012)Competitive immunoassayBefore 11.00 AMAverage 2.2 years ± 1.6 (0.2–5.4)≤10 nmol/lKF:
testosterone 21543 immunoassayBefore 11.00 AMAverage 2.2 years ± 1.6 (0.2–5.4)≤10 nmol/lKF: n = 5NOA: n = 40Mean testosterone levels and prevalence low testosteroneAltinkilic (2017)Not described08.00–10.00 AM6 weeksNot describedbefore
testosterone 21582 years ± 1.6 (0.2–5.4)≤10 nmol/lKF: n = 5NOA: n = 40Mean testosterone levels and prevalence low testosterone Altinkilic (2017)Not described08.00–10.00 AM6 weeksNot describedbefore TESE: n = 78after TESE: n =
testosterone 21702 testosteroneAltinkilic (2017)Not described08.00–10.00 AM6 weeksNot describedbefore TESE: n = 78after TESE: n = 67Mean testosterone levelsBinsaleh (2017)Not describedNot reported3 months and more than 1 yearNot described111Mean testosterone
testosterone 21811 testosterone levelsBinsaleh (2017)Not describedNot reported3 months and more than 1 yearNot described111Mean testosterone levels*Not included in meta-regression analysis.Figure 3Overview of mean serum total testosterone levels
testosterone 21909 described111Mean testosterone levels*Not included in meta-regression analysis.Figure 3Overview of mean serum total testosterone levels in men after TESE over time. Total testosterone levels are shown in (A) all men, (B) men with
testosterone 21964 analysis.Figure 3Overview of mean serum total testosterone levels in men after TESE over time. Total testosterone levels are shown in (A) all men, (B) men with Klinefelter syndrome and (C) men with non-obstructive
testosterone 22225 in total data for 54 men were available ([38]; [19]; [6]). There was a significant decrease in total testosterone levels after TESE, but these levels recovered to baseline values after 26 months (Fig. 3B). In one out
testosterone 22368 levels recovered to baseline values after 26 months (Fig. 3B). In one out of three studies, the mean testosterone levels in men with Klinefelter syndrome were above the threshold for hypogonadism of 12 nmol/l at baseline
testosterone 22579 baseline ([6]). The meta-analysis using mean differences shows the strongest mean decrease in total testosterone at 6 months after TESE with a mean decrease of 4.13 nmol/l (95% CI: −5.86, −2.40) (Supplementary
testosterone 22719 a mean decrease of 4.13 nmol/l (95% CI: −5.86, −2.40) (Supplementary Fig. S1A). The mean total testosterone levels rose at long-term follow-up (>12 months) to a mean difference of −2.28 nmol/l (95% CI: −4.03,
testosterone 22861 follow-up (>12 months) to a mean difference of −2.28 nmol/l (95% CI: −4.03, −0.53), but the total testosterone levels remained significantly lower compared to the levels before TESE.For men with NOA we were able
testosterone 23110 total of 252 men ([23]; [38]; [19]; [26]; [6]). In these men we found variations in baseline mean total testosterone levels with some mean total testosterone levels below the threshold for hypogonadism of 12 nmol/l (Fig.
testosterone 23151 [6]). In these men we found variations in baseline mean total testosterone levels with some mean total testosterone levels below the threshold for hypogonadism of 12 nmol/l (Fig. 3C). We found the largest decrease in
testosterone 23276 the threshold for hypogonadism of 12 nmol/l (Fig. 3C). We found the largest decrease in mean total testosterone levels 6 months after TESE, of 2.72 nmol/l (95% CI: −5.02, −0.41) (Supplementary Fig. S1B). Our
testosterone 23446 −5.02, −0.41) (Supplementary Fig. S1B). Our meta-analysis shows a significant decrease in mean total testosterone levels at 9–12 months after TESE, which disappears at long-term follow-up.In most studies LH levels
testosterone 23582 after TESE, which disappears at long-term follow-up.In most studies LH levels were associated with testosterone levels; when a decrease in total testosterone was reported, a significant increase in LH was found ([38];
testosterone 23628 follow-up.In most studies LH levels were associated with testosterone levels; when a decrease in total testosterone was reported, a significant increase in LH was found ([38]; [2]; [5]) and when no decrease in total
testosterone 23741 was reported, a significant increase in LH was found ([38]; [2]; [5]) and when no decrease in total testosterone was reported, also no increase in LH was found ([34]; [18]; [6]). In one study no decrease in serum
testosterone 23854 was reported, also no increase in LH was found ([34]; [18]; [6]). In one study no decrease in serum testosterone after TESE in men with NOA and OA was reported, but an increase in LH levels after TESE was seen ([19]).
testosterone 24044 after TESE was seen ([19]). In the same study ([19]) in men with Klinefelter syndrome a decrease in testosterone after TESE was reported, but no increase in LH levels.One study examined Leydig cell function by performing
testosterone 24267 hCG test within a period of 4–32 months after TESE ([29]). Out of 13 men with NOA with low serum testosterone levels measured before or after TESE, three men had insufficient increase in testosterone levels after
testosterone 24357 low serum testosterone levels measured before or after TESE, three men had insufficient increase in testosterone levels after stimulation with hCG (<1.5-fold increase). In addition, 6 out of 15 men with NOA with normal
testosterone 24476 after stimulation with hCG (<1.5-fold increase). In addition, 6 out of 15 men with NOA with normal testosterone levels before and after TESE showed insufficient testosterone increase after hCG stimulation, indicating
testosterone 24538 6 out of 15 men with NOA with normal testosterone levels before and after TESE showed insufficient testosterone increase after hCG stimulation, indicating a disturbed functioning of Leydig cells.Prevalence of low
testosterone 24652 increase after hCG stimulation, indicating a disturbed functioning of Leydig cells.Prevalence of low testosterone after TESEFive studies described the prevalence of low total testosterone levels after TESE, using thresholds
testosterone 24726 Leydig cells.Prevalence of low testosterone after TESEFive studies described the prevalence of low total testosterone levels after TESE, using thresholds varying from 5 to 12 nmol/l, or this was not specified. In total,
testosterone 24961 involved (Table III). The ORs per study show that there is a trend towards an increased risk for low total testosterone levels after TESE (Fig. 4). Because of the differences in follow-up time and in thresholds used for
testosterone 25078 levels after TESE (Fig. 4). Because of the differences in follow-up time and in thresholds used for low testosterone levels, pooling of the data was not informative.Figure 4Forest plot with odds ratio of low total testosterone
testosterone 25188 testosterone levels, pooling of the data was not informative.Figure 4Forest plot with odds ratio of low total testosterone in men after TESE.Risk of symptoms and signs related to hypogonadism after TESEOur systematic literature
testosterone 27949 36 men, but only the data of the 13 men with new-onset ED are reported. In these men the mean total testosterone level was significantly decreased from 27.1 to 9.7 nmol/l. LH was increased in these men, but not significantly.
testosterone 31242 high quality data are available from literature. We found there is a temporary decrease in serum total testosterone levels after TESE, for at least 1 year, with levels that may decrease below 12 nmol/l, a threshold level
testosterone 31676 testicular size.Testosterone as a measure for hypogonadismAll included studies presented data on serum total testosterone , one of the measures to determine hypogonadism. The decrease in mean serum total testosterone levels
testosterone 31770 total testosterone, one of the measures to determine hypogonadism. The decrease in mean serum total testosterone levels was most profound 6 months after TESE and recovered again to baseline levels after 18 months
testosterone 31999 as well as in men with Klinefelter syndrome. Overall, we saw a greater effect of TESE on mean total testosterone levels in men with Klinefelter syndrome compared to men with NOA. Men with Klinefelter syndrome have
testosterone 32129 with Klinefelter syndrome compared to men with NOA. Men with Klinefelter syndrome have decreased basal testosterone levels during and after puberty ([28]). Because of their low baseline levels, these men might be more
testosterone 32271 puberty ([28]). Because of their low baseline levels, these men might be more sensitive to a decrease in testosterone levels after TESE. Another explanation is that in men with Klinefelter syndrome the testicular volume
testosterone 32654 subsequently the area of tissue that is damaged will be higher.Interpretation of the consequence of low testosterone levels is not straightforward in view of the different cut-off values suggested by different professional
testosterone 33115 are associated with symptoms related to hypogonadism ([14]). At 6 months after TESE, the mean total testosterone levels of men with Klinefelter syndrome were 4.5–6.3 nmol/l and for men with NOA, 8.7–16.4 nmol/l.
testosterone 33315 8.7–16.4 nmol/l. This implies that in men with Klinefelter and in a proportion of men with NOA total testosterone levels drop below the threshold of 12 nmol/l and thus have a risk of developing symptoms and signs associated
testosterone 33513 symptoms and signs associated with hypogonadism after TESE.We expect the highest prevalence of low total testosterone levels 6 months after TESE, because of the fact that we see the most profound decrease in mean total
testosterone 33627 levels 6 months after TESE, because of the fact that we see the most profound decrease in mean total testosterone levels at this time point. Two out of five studies measured the prevalence at 6 months and these two
testosterone 33759 point. Two out of five studies measured the prevalence at 6 months and these two studies found low testosterone levels in 53 and 5% of the men ([23]; [25]). However, [23] did not report the threshold used, while
testosterone 33968 while [25] used a very low threshold of 4.9 nmol/l. The other studies that measured prevalence of low testosterone used a follow-up time varying from 1 to 26 months after TESE.Clinical signs and symptoms of hypogonadismPatients
testosterone 34162 symptoms of hypogonadismPatients will experience hypogonadism by their symptoms rather than on serum testosterone levels. Although cut-off values of serum testosterone levels help to diagnose hypogonadism after TESE,
testosterone 34216 hypogonadism by their symptoms rather than on serum testosterone levels. Although cut-off values of serum testosterone levels help to diagnose hypogonadism after TESE, it is not clear whether the TESE-induced decrease in
testosterone 34337 help to diagnose hypogonadism after TESE, it is not clear whether the TESE-induced decrease in total testosterone levels, irrespective of the levels of serum total testosterone before TESE, might lead to hypogonadism.
testosterone 34400 whether the TESE-induced decrease in total testosterone levels, irrespective of the levels of serum total testosterone before TESE, might lead to hypogonadism. Therefore, symptoms are more clinically relevant in order to
testosterone 34682 out of 66 men at 6 months after TESE. This was accompanied by a significant decrease in mean total testosterone levels below 12 nmol/l. This suggests that ED after TESE might be explained by hypogonadism, although
testosterone 34885 hypogonadism, although we cannot exclude that ED is caused by psychological reasons instead of decreased total testosterone levels. ED was especially found in the group of men with unsuccessful sperm retrieval, depression and
testosterone 35374 possibly more biopsies are taken from these men. This might contribute to a higher risk of a decrease in testosterone levels and therefore ED ([23]).An effect of TESE on testicular volume was seen in studies at 6 weeks
testosterone 36017 a cohort of 54 men with Klinefelter syndrome and 252 men with NOA, we can conclude that serum total testosterone levels decrease after TESE surgery to levels that might be related to symptoms and signs for hypogonadism.
testosterone 36580 addition, the small size of the available cohorts. Furthermore, most studies only reported on serum total testosterone levels. Strikingly, although TESE is routinely applied, there are only follow-up data available for
testosterone 36935 these numbers are not representative for all time-points. Furthermore, although more data on total testosterone levels after TESE were available, not all studies reported the data separately for men with different
testosterone 37359 this study are in line with our results of the meta-analysis.The effect of TESE on decreased total testosterone levels is based on mean total testosterone levels and, because of this, the observed effects may be
testosterone 37402 the meta-analysis.The effect of TESE on decreased total testosterone levels is based on mean total testosterone levels and, because of this, the observed effects may be an underestimation in individuals. A decrease
testosterone 37527 because of this, the observed effects may be an underestimation in individuals. A decrease in total testosterone levels in individuals could be missed when looking at the mean levels of a cohort. Therefore, normal
testosterone 37652 individuals could be missed when looking at the mean levels of a cohort. Therefore, normal mean total testosterone levels do not rule out the presence of men with total testosterone levels below 12 nmol/l that are at
testosterone 37719 cohort. Therefore, normal mean total testosterone levels do not rule out the presence of men with total testosterone levels below 12 nmol/l that are at risk for symptoms of hypogonadism.Although we were able to do a separate
testosterone 38128 differs between various causes of subfertility. In line with this it was shown that the prevalence of low testosterone levels in general in men with NOA is reported to be 45%, while in men with OA this is 16.7% ([36]).
testosterone 38260 in men with NOA is reported to be 45%, while in men with OA this is 16.7% ([36]). In addition, lower testosterone baseline levels for men with maturation arrest and Sertoli cell only syndrome were found compared to
testosterone 39444 needle, the location is less well identified. In the three studies comparing the decrease in total testosterone levels after conventional TESE with that after microdissection TESE, the risk was higher or comparable
testosterone 39931 the data between the studies.Biological interpretations of the evidenceThe effect of TESE on total testosterone can be explained by different mechanisms. The first explanation is that part of the testicular tissue
testosterone 40137 testicular tissue is removed resulting in a lower number of Leydig cells and therefore a lower production of testosterone . However, with decreased serum testosterone levels, the remaining Leydig cells will be stimulated by
testosterone 40181 number of Leydig cells and therefore a lower production of testosterone. However, with decreased serum testosterone levels, the remaining Leydig cells will be stimulated by higher LH levels due to the negative feedback
testosterone 40391 feedback in the hypothalamus–pituitary–gonad axis, and they should become more active in producing testosterone . Nevertheless, it has been shown that stimulation of Leydig cells with hCG after TESE in men with low
testosterone 40506 Nevertheless, it has been shown that stimulation of Leydig cells with hCG after TESE in men with low testosterone levels showed an adequate response, with increased testosterone levels 3 and 4 days after hCG injection.
testosterone 40570 with hCG after TESE in men with low testosterone levels showed an adequate response, with increased testosterone levels 3 and 4 days after hCG injection. Therefore, these Leydig cells are able to produce more testosterone
testosterone 40679 testosterone levels 3 and 4 days after hCG injection. Therefore, these Leydig cells are able to produce more testosterone when they are stimulated, suggesting that in these men a more systemic cause of low LH levels could
testosterone 41049 some studies showed an increase in LH levels after TESE, the normal correlation between LH and total testosterone was not always observed. In one study high LH levels and normal testosterone levels were found in men
testosterone 41126 correlation between LH and total testosterone was not always observed. In one study high LH levels and normal testosterone levels were found in men with NOA and OA ([19]). This combination of high LH and normal testosterone
testosterone 41227 testosterone levels were found in men with NOA and OA ([19]). This combination of high LH and normal testosterone levels is called compensated hypogonadism and might lead to hypogonadism in the future ([37]). At this
testosterone 41417 the future ([37]). At this point Leydig cells need a higher stimulation to be able to produce normal testosterone levels. However, the number of reports on LH concentrations in relation to testosterone concentrations
testosterone 41505 produce normal testosterone levels. However, the number of reports on LH concentrations in relation to testosterone concentrations after TESE is limited and further research would give more insights in the various forms
testosterone 41684 give more insights in the various forms of hypogonadism.A second explanation of the recovery of total testosterone levels is related to the time to repopulate Leydig cells by stem Leydig cells and therefore restore
testosterone 41797 levels is related to the time to repopulate Leydig cells by stem Leydig cells and therefore restore testosterone production at 18 month after TESE. In the rat testis it takes 21 days for new adult Leydig cells to
testosterone 42274 possibility is that the number and function of the Leydig cells is not the cause of decreased total testosterone levels after TESE, but that this is induced by vascular damage in the testis. This vascular damage can
testosterone 42497 in lower stimulation of Leydig cells by LH because it cannot reach the Leydig cells efficiently, or testosterone is produced in the testis at normal levels but cannot be released into the blood circulation. Indeed,
testosterone 43007 systematic search, based on the extracted data we found transient but significantly decreased total testosterone levels after TESE that recover to baseline levels after 18–26 months. This effect was most profound
testosterone 43336 with TESE is very limited, showing some risk of ED, which seems to be related to a decreased total testosterone and/or possible depression and anxiety. Furthermore, a decrease in testicular volume is seen in some
testosterone 43616 transient hypogonadism after TESE, more research is necessary to understand whether the decreased total testosterone is accompanied by symptoms and signs of hypogonadism in the short and long term. It is striking that
Select Disease Character Offset Disease Term Instance
diabetes mellitus 7267 energy/fatigue/sleep disturbances/increased sleepinessMetabolic syndromeInsulin resistance and type-2 diabetes mellitus Diminished cognitive function/poor concentration and memory, diminished physical or work performanceMild
hypogonadism 57 Title: Human Reproduction UpdateThe risk of TESE-induced hypogonadism : a systematic review and meta-analysisJitske EliveldMadelon van WelyAndreas MeißnerSjoerd ReppingFulco
hypogonadism 822 inflammation and a decrease in testosterone levels have been described as such. The prevalence and duration of hypogonadism and associated symptoms after TESE have not been studied systematically.OBJECTIVE AND RATIONALEIn this
hypogonadism 1157 and, if so, do these levels recover over time? What is the prevalence of symptoms and signs related to hypogonadism after TESE and are they related to testosterone levels?SEARCH METHODSWe searched the databases Pubmed
hypogonadism 1613 used, that measured testosterone and/or LH, and/or had information on signs or symptoms related to hypogonadism as defined by hypogonadism guidelines. An additional inclusion criterion was that studies described
hypogonadism 1640 testosterone and/or LH, and/or had information on signs or symptoms related to hypogonadism as defined by hypogonadism guidelines. An additional inclusion criterion was that studies described these measurements both before
hypogonadism 2511 testosterone concentrations below a cut-off value of 12 nmol/l, where symptoms and signs related to hypogonadism may appear. Furthermore, an increased prevalence of erectile dysfunction related to decreased total
hypogonadism 2972 significant, decrease in total testosterone levels indicates that men are at risk of developing a temporary hypogonadism after TESE, but there is insufficient evidence for whether patients actually experience clinical symptoms
hypogonadism 3238 To be able to properly counsel TESE patients, more large-scale monitoring on signs and symptoms of hypogonadism , in combination with testosterone measurements, needs to be performed in men undergoing TESE.IntroductionTesticular
hypogonadism 5670 TESE procedure has been described ([15]; [33]). Decreased testosterone levels can subsequently lead to hypogonadism . Symptoms of hypogonadism have been described to occur more often when total testosterone levels are
hypogonadism 5696 described ([15]; [33]). Decreased testosterone levels can subsequently lead to hypogonadism. Symptoms of hypogonadism have been described to occur more often when total testosterone levels are below a threshold of 12 nmol/l,
hypogonadism 5895 threshold of 12 nmol/l, and the lower the total testosterone values, the more frequent the symptoms of hypogonadism will be present ([4]; [14]; [44]).According to various guidelines on hypogonadism, the diagnosis is
hypogonadism 5977 frequent the symptoms of hypogonadism will be present ([4]; [14]; [44]).According to various guidelines on hypogonadism , the diagnosis is based on the presence of one or more signs or symptoms. Symptoms can be—among others—erectile
hypogonadism 6376 occur (Table I) ([42]; [3]; [21]). Because many of these clinical manifestations are not specific for hypogonadism , the diagnosis should always be confirmed by measuring serum testosterone levels ([3]; [14]). Table
hypogonadism 7427 concentration and memory, diminished physical or work performanceMild anaemiaThe prevalence and duration of hypogonadism and associated symptoms as a result of the TESE procedure have not been studied systematically. This
hypogonadism 7647 information is necessary to properly counsel men who qualify for TESE on the potential risk of developing hypogonadism after TESE. We therefore systematically reviewed the literature and included all studies that measured
hypogonadism 7831 included all studies that measured testosterone levels, LH levels and/or signs and symptoms related to hypogonadism before and after TESE. In this systematic review we addressed the following research questions: Are
hypogonadism 8100 and, if so, do these levels recover over time? What is the prevalence of symptoms and signs related to hypogonadism after TESE and are they related to total testosterone levels?MethodsThis review is reported according
hypogonadism 9532 techniques. We included all studies which measured testosterone, LH, or signs or symptoms related to hypogonadism (Table I), defined according to international hypogonadism guidelines ([3]; [14]; [42]). To assess the
hypogonadism 9591 testosterone, LH, or signs or symptoms related to hypogonadism (Table I), defined according to international hypogonadism guidelines ([3]; [14]; [42]). To assess the association between TESE and hypogonadism and its associated
hypogonadism 9677 international hypogonadism guidelines ([3]; [14]; [42]). To assess the association between TESE and hypogonadism and its associated signs and symptoms, we only included the studies that performed the measurements
hypogonadism 12638 flowchart is depicted in Fig. 1.Figure 1Flowchart of the search and selection of literature on induced hypogonadism after testicular sperm extraction in men. TESE, testicular sperm extraction.Study characteristicsAll
hypogonadism 12934 after TESE. Nine studies also reported serum LH levels and six studies reported on symptoms or signs of hypogonadism in addition to the hormone levels (Table II). The 15 studies were published between 1998 and 2017. The
hypogonadism 19976 testosterone level was normal before TESE and after TESE <1.4 ng/ml or a decrease >1 ng/ml for men with hypogonadism before TESEConventional TESE: n = 40microdissection TESE: n = 80Prevalence significant decrease in testosterone
hypogonadism 22450 studies, the mean testosterone levels in men with Klinefelter syndrome were above the threshold for hypogonadism of 12 nmol/l at baseline ([6]). The meta-analysis using mean differences shows the strongest mean decrease
hypogonadism 23195 baseline mean total testosterone levels with some mean total testosterone levels below the threshold for hypogonadism of 12 nmol/l (Fig. 3C). We found the largest decrease in mean total testosterone levels 6 months after
hypogonadism 25257 plot with odds ratio of low total testosterone in men after TESE.Risk of symptoms and signs related to hypogonadism after TESEOur systematic literature search revealed that only six studies reported on symptoms or signs
hypogonadism 25390 systematic literature search revealed that only six studies reported on symptoms or signs associated with hypogonadism after TESE (Table IV). The reported symptoms and signs are limited to ED ([1]) and changes in testicular
hypogonadism 25628 [25]; [26]; [29]). Table IVBasic characteristics of studies that measured symptoms or signs related to hypogonadism after TESE.First author (year of publication)Type of measurementTechnique of measurementTime after TESENumber
hypogonadism 27062 3.7 ml, right: 7.5 ± 4.6 mlRisk of ED after TESEThe risk of ED after TESE, one of the symptoms of hypogonadism , was described in one study in which 13 out of 66 men with new-onset ED were reported 6 months after
hypogonadism 28420 procedure or a cause of the ED.Risk of decrease in testis volume after TESEOne of the signs associated with hypogonadism is a decrease in testis volume. Five studies reported on this sign before and after TESE ([2]; [25];
hypogonadism 31063 TESE did not measure the testis volume in all men before TESE.DiscussionIn this review we evaluated hypogonadism in men with azoospermia after TESE surgery and showed that few high quality data are available from
hypogonadism 31445 threshold level for risk of becoming hypogonadal. The available information on signs and symptoms of hypogonadism after TESE suggests that some men may experience ED, together with depression and anxiety, and a decrease
hypogonadism 31613 together with depression and anxiety, and a decrease in testicular size.Testosterone as a measure for hypogonadism All included studies presented data on serum total testosterone, one of the measures to determine hypogonadism.
hypogonadism 31723 hypogonadismAll included studies presented data on serum total testosterone, one of the measures to determine hypogonadism . The decrease in mean serum total testosterone levels was most profound 6 months after TESE and recovered
hypogonadism 32903 According to the Endocrine Society, levels lower than 10.4 nmol/l can be regarded as associated with hypogonadism ([3]). On the other hand, the European Association of Urology suggests that levels below 12 nmol/l are
hypogonadism 33055 Association of Urology suggests that levels below 12 nmol/l are associated with symptoms related to hypogonadism ([14]). At 6 months after TESE, the mean total testosterone levels of men with Klinefelter syndrome
hypogonadism 33443 below the threshold of 12 nmol/l and thus have a risk of developing symptoms and signs associated with hypogonadism after TESE.We expect the highest prevalence of low total testosterone levels 6 months after TESE, because
hypogonadism 34073 testosterone used a follow-up time varying from 1 to 26 months after TESE.Clinical signs and symptoms of hypogonadism Patients will experience hypogonadism by their symptoms rather than on serum testosterone levels. Although
hypogonadism 34110 from 1 to 26 months after TESE.Clinical signs and symptoms of hypogonadismPatients will experience hypogonadism by their symptoms rather than on serum testosterone levels. Although cut-off values of serum testosterone
hypogonadism 34253 on serum testosterone levels. Although cut-off values of serum testosterone levels help to diagnose hypogonadism after TESE, it is not clear whether the TESE-induced decrease in total testosterone levels, irrespective
hypogonadism 34440 testosterone levels, irrespective of the levels of serum total testosterone before TESE, might lead to hypogonadism . Therefore, symptoms are more clinically relevant in order to diagnose patients for hypogonadism. New-onset
hypogonadism 34537 to hypogonadism. Therefore, symptoms are more clinically relevant in order to diagnose patients for hypogonadism . New-onset ED was measured in 13 out of 66 men at 6 months after TESE. This was accompanied by a significant
hypogonadism 34774 mean total testosterone levels below 12 nmol/l. This suggests that ED after TESE might be explained by hypogonadism , although we cannot exclude that ED is caused by psychological reasons instead of decreased total testosterone
hypogonadism 35140 resulted in the ED. However, depression and anxiety can, in addition to causing ED, also be symptoms of hypogonadism . Another possible explanation of the higher prevalence of ED in the group with unsuccessful sperm retrieval
hypogonadism 35838 of this systematic reviewThis review is the first to combine all the reported data on TESE-induced hypogonadism . Because we were able to pool data from these studies, leading to a cohort of 54 men with Klinefelter
hypogonadism 36123 testosterone levels decrease after TESE surgery to levels that might be related to symptoms and signs for hypogonadism . This was supported by the prevalence of new-onset ED and the occurrence of decreased testicular volume
hypogonadism 37788 the presence of men with total testosterone levels below 12 nmol/l that are at risk for symptoms of hypogonadism .Although we were able to do a separate analysis for men with Klinefelter syndrome and men with NOA,
hypogonadism 38009 not able to study the group of men with OA with the available data. It is possible that the risk of hypogonadism differs between various causes of subfertility. In line with this it was shown that the prevalence of
hypogonadism 40805 stimulated, suggesting that in these men a more systemic cause of low LH levels could underlie the hypogonadism after TESE. Indeed, when LH was upregulated immediately after TESE a faster recovery than 18 months
hypogonadism 41269 NOA and OA ([19]). This combination of high LH and normal testosterone levels is called compensated hypogonadism and might lead to hypogonadism in the future ([37]). At this point Leydig cells need a higher stimulation
hypogonadism 41300 combination of high LH and normal testosterone levels is called compensated hypogonadism and might lead to hypogonadism in the future ([37]). At this point Leydig cells need a higher stimulation to be able to produce normal
hypogonadism 41625 concentrations after TESE is limited and further research would give more insights in the various forms of hypogonadism .A second explanation of the recovery of total testosterone levels is related to the time to repopulate
hypogonadism 43213 profound in men with Klinefelter syndrome. The number of studies reporting on symptoms and signs of hypogonadism associated with TESE is very limited, showing some risk of ED, which seems to be related to a decreased
hypogonadism 43522 testicular volume is seen in some men after TESE.For better counselling of TESE patients on the transient hypogonadism after TESE, more research is necessary to understand whether the decreased total testosterone is accompanied
hypogonadism 43669 necessary to understand whether the decreased total testosterone is accompanied by symptoms and signs of hypogonadism in the short and long term. It is striking that these data are still not available 25 years after the
obesity 6780 erectionsGynaecomastia/breast discomfortDecrease in lean body mass and muscle strength/reduced muscle bulkVisceral obesity /increased body fat, BMIDecrease in bone mineral density (osteoporosis) with low trauma fractures/height
osteoporosis 6845 strength/reduced muscle bulkVisceral obesity/increased body fat, BMIDecrease in bone mineral density ( osteoporosis ) with low trauma fractures/height lossReduced sexual desire and sexual activity/reduced libidoDecreased

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