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Table of Contents
ORIGINAL ARTICLE
Year : 2019  |  Volume : 30  |  Issue : 3  |  Page : 118-123

The impact of obesity on serum testosterone levels and semen quality in a population of infertile men


1 Division of Urology, National Taiwan University Hospital; Department of Surgery, Division of Urology, Cardinal Tien Hospital, Taipei, Taiwan
2 Division of Urology, National Taiwan University Hospital, Taipei, Taiwan
3 Department of Surgery, Division of Urology, Cardinal Tien Hospital; Department of Surgery, Division of Urology, Fu Jen Catholic University Hospital, Taipei, Taiwan

Date of Submission07-Nov-2018
Date of Decision11-Jan-2019
Date of Acceptance25-Jan-2019
Date of Web Publication20-Jun-2019

Correspondence Address:
Hung-Chiang Chang
Department of Urology, National Taiwan University, No. 7, Zhongshang South Road, Taipei City 100
Taiwan
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/UROS.UROS_132_18

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  Abstract 


Introduction: Multiple factors contribute to male infertility, with hypogonadism and low testosterone levels possibly affecting fertility in different aspects. This study focused on factors for low testosterone in infertile male patients. Materials and Methods: We retrospectively collected data of patients who were diagnosed with infertility and visited the National Taiwan University Hospital from January 2015 to October 2017. Patients' weight and height, basic blood test results, sperm analysis, and sex hormone profile were recorded. Patients diagnosed with obstructive azoospermia, particularly absence of bilateral vas deferens, those who received a vasectomy or orchiectomy, and patients diagnosed with cancer undergoing chemotherapy or radiotherapy were excluded. Pearson's correlation test was applied for detecting associating factors for serum testosterone. Multivariate linear regression was used for detecting independent factors predicting serum testosterone. An independent t-test was used to analyze continuous variables, and the Chi-square test was used for categorical variables. Results: Two hundred and forty-seven patients had serum sex hormone profile and semen profile recorded. The mean age was 36.48 ± 8.68 years. Pearson's correlation test showed that serum testosterone was correlated with serum triglyceride, total cholesterol, fasting blood sugar, and body mass index (BMI). However, multivariate linear regression showed BMI (P = 0.001) and smoking (P = 0.029) to be independent factors predicting serum testosterone. On comparing sex hormone profile and semen profile between obese (BMI ≥30), overweight patient (BMI ≥25, <30), and nonoverweight patients (BMI <25), (i) serum testosterone was significantly lower in the obese and overweight group comparing to nonoverweight group (nonoverweight: 3.61 ± 1.63 ng/ml vs. overweight: 2.87 ± 1.27, P = 0.001; nonoverweight: 3.61 ± 1.63 vs. obese 2.89 ± 1.59, P = 0.035). Follicle stimulating hormone, luteinizing hormone, and prolactin did not differ significantly between the groups. No significant difference in sperm parameters, namely the total sperm count, sperm concentration, total sperm motility, and morphology, was observed between the groups. Conclusion: In the infertile Taiwanese male population, obese patients (BMI ≥ 30) and overweight patients (BMI ≥25) had a significant lower serum testosterone than the nonoverweight patients. Body weight control and treatment of metabolic syndrome, and diabetes could improve serum testosterone levels.

Keywords: Infertility, obesity, testosterone


How to cite this article:
Chen YA, Chang HC, Liao CH. The impact of obesity on serum testosterone levels and semen quality in a population of infertile men. Urol Sci 2019;30:118-23

How to cite this URL:
Chen YA, Chang HC, Liao CH. The impact of obesity on serum testosterone levels and semen quality in a population of infertile men. Urol Sci [serial online] 2019 [cited 2019 Dec 16];30:118-23. Available from: http://www.e-urol-sci.com/text.asp?2019/30/3/118/260779




  Introduction Top


Infertility is a major problem for married couples in both developing and developed countries. According to a systematic review, the prevalence of infertility is estimated to be 15% globally, and male infertility was reported to account for 20%–70% of infertility cases.[1] The prevalence of infertility has been reported to be stable or increasing during the present decade, based on the findings of different cohorts.[2],[3]

Infertility is a multifactorial problem with no single cause. The causes of male infertility include poor sperm quality, chromosomal errors, and environmental factors, such as lifestyle and habits. Hypogonadism is also a cause of male infertility.[4],[5]

In terms of hormonal imbalance, a low testosterone level can affect fertility in different aspects. A low testosterone level is associated with decreased libido and sexual desire [6] and poor semen motility, progressive motility, and morphology.[7] Pavlovich et al. reported that infertile men with poor spermatogenesis had a decreased testosterone-to-estrogen ratio compared with those with normal spermatogenesis. The administration of aromatase anastrozole (1 mg/day) or letrozole (2.5 mg/day) inhibitor to patients with poor spermatogenesis and a decreased testosterone-to-estrogen ratio could improve to elevate their testosterone level and spermatogenesis.[8],[9]

In this study, we focused on metabolic risk factors for a lower than normal testosterone level in infertile men. If these factors are found to be reversible, correcting them would enable such patients to recover from hypogonadism and recover fertility.


  Materials and Methods Top


Patients

We retrospectively collected patients who were diagnosed with infertility and visited the National Taiwan University Hospital from January 2015 to October 2017. A total of 247 patients had their semen profile and sex hormone profile recorded and were further analyzed.

Their weight, height, basic blood test results, sperm analysis results, and if necessary for planning further treatment sex hormone profile were recorded. In addition, we recorded their age and the duration between the onset of infertility and their first visit to the urological clinic. For patients who received more than one semen analysis, the first data collected before treatment were recorded and analyzed. Patients who had aberrant chromosomes, who received chemotherapy or radiotherapy for malignancies, or who underwent bone marrow transplantation were excluded. Patients diagnosed with obstructive azoospermia, particularly absence of bilateral vas deferens, those who received a vasectomy or orchiectomy, and those diagnosed with cancer undergoing chemotherapy or radiotherapy were excluded.

Semen analysis was performed by an experienced team. Patients were requested to abstain from sex for 3–5 days. Patients submitted a sperm sample obtained through masturbation to our laboratory within 2 hours. The samples then underwent microscopic examination, and the semen volume and sperm concentration and morphology were also recorded.

Statistical analysis

The statistical analysis was performed with SPSS version 12 (SPSS Inc., Chicago, IL, USA).

Pearson's correlation coefficient was applied for detection factors correlating to serum testosterone. Then, multivariate linear regression model was used to detect independent variable for testosterone level.

We classified overweight patients as those with a body mass index (BMI) of ≥25, as defined by the WHO. Semen parameters and hormone profile were compared between the groups. Independent t-test and Chi-square test were used for examining continuous variables and categorical variables, respectively.


  Results Top


The demographics of the patients are shown in [Table 1]. The mean age of our patients was 36.48 (±8.68) years. The mean BMI was 24.79 (±3.64). The mean follicle stimulating hormone (FSH), luteinizing hormone (LH), testosterone, and prolactin were 11.2 (±10.8) ng/ml, 5.89 (±4.43) ng/ml, 3.3 (±1.55) ng/ml, and 9.5 (±6.37) ng/ml, respectively.
Table 1: Demographic of the patients recruited in the study (n=247)

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Pearson's correlation coefficients were calculated, revealing that the BMI, fasting blood glucose level, total blood cholesterol level, and blood triglyceride level were inversely correlated to the serum testosterone level [Table 2]. Moreover, BMI (negatively correlates with serum testosterone, P < 0.0001) and nicotine consumption (smoker had higher serum testosterone, P = 0.029) showed significant correlation with serum testosterone on the multivariate linear regression [Table 3].
Table 2: Pearson's correlation coefficients

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Table 3: Multivariate linear regression for serum testosterone

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The patients were divided into three groups, obese (BMI ≥30), overweight (BMI ≥25, <30), and nonoverweight (BMI <25), as defined by the WHO. A total of 28 patients (11.34%) were obese, 76 (31.2%) were overweight, and 143 (57.9%) were not overweight. The patients' mean age was 36.54 (±8.736) years.

The mean age of the obese, overweight, and nonoverweight groups was 37.25 (±7.834), 37.33 (±8.72), and 35.98 (±8.92) years, respectively (P > 0.05). The mean age of the sexual partner, mean fasting glucose, serum triglyceride, and total cholesterol between the three groups did not differ significantly.

The mean FSH, LH, and prolactin level between the two groups did not differ significantly as well [Table 4]. However, there was a trend of lower FSF and LH level in the overweight patients and even lower in the obese group. Nevertheless, the mean serum testosterone level differed significantly between nonoverweight and overweight patients (3.61 ± 1.63 ng/ml vs. 2.87 ± 1.27, P = 0.001) and between nonoverweight and obese patients (3.61 ± 1.63 vs. 2.89 ± 1.59, P = 0.035). The difference was not significant between overweight patients and obese patients though (P = 0.934).
Table 4: Demographics of patients with body mass index ≥ 30, 30>body mass index ≥ 25, and body mass index <25

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No significant difference in sperm parameters, namely the total sperm count, sperm concentration, total sperm motility, and sperm morphology, was observed between the three groups.


  Discussion Top


Studies have reported a link among obesity, metabolic syndrome, and altered serum sex hormone levels, especially the testosterone level.[10],[11] MacDonald et al., who recruited patients from a fertility clinic in New Zealand, found that higher BMI was associated with a lower serum testosterone level. Although these patients had not necessarily been diagnosed with infertility, many of them may have been subfertile.[12]

A study of general population in Austria showed that men with low serum testosterone levels had an increased risk of glucose intolerance or diabetes, regardless of age and BMI.[2] By contrast, Ho et al. reported a link between prediabetes and a low testosterone level that was independent of obesity and metabolic syndrome.[13] Liu et al. reported that obesity and diabetes were independent risk factors for androgen deficiency.[14] Overall, both obesity and impaired glucose tolerance could affect fertility and infertility is linked to them.

In this study, we found that the fasting blood glucose level was inversely correlated with the serum testosterone level in the infertile male population and was an independent factor for a low serum testosterone level, as demonstrated by Pearson's correlation coefficients and multivariate linear regression results.

In our study, we found that BMI correlated inversely with the serum testosterone level, and the relation was also revealed by the results of linear regression. To further evaluate the finding, a scatter plot for the serum testosterone level and BMI showed that nearly all patients with BMI >25 had serum testosterone levels of <5 ng/mL. The point where a sudden decrease in the serum testosterone level is that when BMI approximates the cutoff value for overweightness, as defined by the WHO, resulted in a nonlinear plot. Consequently, we compared sex hormone profiles and semen parameters between the obese (BMI ≥30), overweight (BMI ≥ 25, <30), and nonoverweight (BMI <25) groups and found that the infertile Taiwanese men in the obese and overweight group had a significantly lower serum testosterone level. However, no significant difference in semen quality was observed between the groups. In addition, the finding that serum testosterone did not differ significantly between overweight and obese patients could be illustrated by the scatter plot.

Obesity had been recognized to be negatively correlated with serum testosterone for >30 years. An observational study conducted in Europe consisting of 3369 men aged 40–79 years showed that obesity was associated with secondary hypogonadism.[15] Similar results were observed in a cross-sectional study in China and Australia. The former showed that BMI negatively correlates with total testosterone, and sex hormone-binding globulin, and the latter showed that obese men had lower total testosterone and calculated free testosterone.[16],[17] In the Taiwanese general population, obesity (BMI ≥27) not only correlates with low serum testosterone but also predicts higher risk of erectile dysfunction and lower sexual desire.[14],[18]

The cause–effect relation between obesity and low testosterone could be bidirectional.

First, testosterone takes part in lipid metabolism. Chronic hypogonadism results in increased adipose tissue and fatty storage from diet with decreased lipolysis.[19],[20] As a result, hypogonadism leads to obesity and decreased body lean mass and insulin resistance.[19],[21],[22] On the other hand, obesity also plays a role in low serum testosterone level, the mechanism for which may due to the disruption of hypothalamic–pituitary axis. Aromatase in excessive adipose tissue of obese patients converts testosterone to estrogen. Estrogen then acts on hypothalamus and pituitary gland, decreasing the release of LH through negative feedback. Consequently, testosterone level further decreases, which perpetuates adipose tissue deposition.[23]

To break the hypogonadal-obesity cycle, several studies had shown that testosterone replacement therapy in hypogonadal patients could increase lean body mass and improve insulin resistance and obesity.[24],[25],[26] Nevertheless, the misuse of testosterone replacement therapy could cause negative consequences. Apart from the increased risk of cardiovascular diseases and the elevation of prostate-specific enzyme,[25],[26] a low testosterone level is also associated with decreased libido and lower sexual activity.[6],[18] Approximately 1.3% of infertile men received testosterone replacement therapy, 88% of whom used replacement therapy for hypogonadism, low libido, or low sexual arousal, as prescribed by an endocrinologist, a general practitioner, a urologist, or a gynecologist.[6],[27] However, the use of testosterone is associated with a decreased sperm count or even azoospermia, with the mean time from initial testosterone supplementation to azoospermia reported to be 8 months.[27],[28] Misuse of testosterone replacement therapy can thus further aggravate infertility.

Apart from self-perpetuating hypogonadal-obesity cycle, disturbed serum testosterone and estrogen levels are also associated with poor semen quality. First, testosterone is crucial in the testicular microenvironment and spermatogenesis, and the local concentration of testosterone is 20–30 folds higher than that of serum.[29] Besides, inappropriately high estrogen level was found to associate with decreased semen parameters.[9],[30]

Moreover, this was demonstrated by the fact that some infertile patients exhibited strong aromatase activity and reflected by a lower testosterone-to-estrogen ratio combined with poor semen quality.[9] After treatment with an aromatase inhibitor, the testosterone level increased and semen quality improved.[9],[27]

Testosterone replacement therapy could increase lean body mass and also treat obesity.[21] However, as mentioned, though androgen replacement may break hypogonadal-obesity cycle, it may result in reduced sperm production.

Treating obesity, metabolic syndrome, and diabetes by means of lifestyle modification, exercise, and weight control could provide better improvement on serum hormone. As shown on previous literature that exercise had positive effect on serum testosterone level,[31],[32] following the improvement of hypogonadism, semen profiles may improve, and perhaps even reverse infertility. The hypogonadal-obesity cycle could be echoed by the finding that there is a trend of lower mean FSH and LH value in the overweight patient and even lower value in the obese patient though the difference was not significant.

Hence, we further divided the patients into two groups, BMI ≥24 and BMI <24, which is the cutoff value of overweight by Taiwanese definition [Table 5] and [Table 6]. Interestingly, a significantly lower FSH and LH level was observed, which echoed the obesity-hypogonadal cycle. A high local regional level of aromatase promotes the transition from testosterone to estrogen and causes a negative feedback on hypothalamus–pituitary axis, lowering the secretion of FSH and LH. Here, testosterone level between the two groups did not differ significantly. Explained by the scatter plot at the value which a dramatic drop of serum testosterone was observed was BMI = 25 [Figure 1].
Table 5: The semen parameter and sex hormone profile of the group

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Table 6: The semen parameter and sex hormone profile of the two groups (body mass index ≥ 24, body mass index <24)

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Figure 1: Scatter plot of serum testosterone (ng/ml) and body mass index

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Finally, we found nicotine consumption to have a positive correlation with serum testosterone by multivariate linear regression. Several studies supported our finding.[33],[34],[35] While some showed no significant testosterone level, difference was shown between smoker and nonsmoker.[36] This relation is still elusive and requires more investigation. Here, we did not elaborate on the cause–effect of smoking and serum testosterone level.

In our study, we found that in Taiwanese infertile male, overweight (BMI ≥25), comparing to those with normal BMI, had significantly lower serum testosterone. The relation between obesity and serum testosterone was also observed in multivariate regression model. Furthermore, this relation between obesity and hypogonadism may work by the negative feedback on hypothalamus–pituitary axis.

Despite those findings, this study still has some limitations.

First, this study was retrospective in nature. We did not have complete lipid, blood glucose, or sex hormone profiles for each patient, and due to missing data, we were unable to further interpret the relationship between the blood sugar, triglyceride, cholesterol, and serum testosterone, since bias could not be avoided with limited case number. Second, due to the retrospective nature of this study, we were unable to obtain the result that if any of those patients successfully fathered a child. Medical treatments given to those patients were mainly hormone replacement therapy. Thirty patients (12.1%) received clomiphene, a selective estrogen receptor modulator which elevates, which was used in male infertility for >50 years. Thirteen patients (5.3%) received human chorionic gonadotropin (HCG) and three patients (1.2%) received testosterone replacement therapy. However, whether their partner successfully conceived was unknown.

To our knowledge, this is the first article focusing on the interaction between obesity and hypogonadism in Taiwanese infertile male. Further prospective study could be carried out to further demonstrate the effect of treating obesity on fertility.


  Conclusion Top


In the infertile Taiwanese male population, obese patients (BMI ≥30) and overweight patients (BMI ≥25) had significant lower serum testosterone than the nonoverweight patients. In additional, BMI ≥24 was associated with a significantly lower FSH and LH level, echoing the obesity-hypogonadal cycle.

Body weight control and treatment of obesity might be beneficial in improving hypogonadism in infertile male.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Agarwal A, Mulgund A, Hamada A, Chyatte MR. A unique view on male infertility around the globe. Reprod Biol Endocrinol 2015;13:37.  Back to cited text no. 1
    
2.
Odisho AY, Nangia AK, Katz PP, Smith JF. Temporal and geospatial trends in male factor infertility with assisted reproductive technology in the United States from 1999-2010. Fertil Steril 2014;102:469-75.  Back to cited text no. 2
    
3.
Zhang H, Wang S, Zhang S, Wang T, Deng X. Increasing trend of prevalence of infertility in Beijing. Chin Med J (Engl) 2014;127:691-5.  Back to cited text no. 3
    
4.
Leaver RB. Male infertility: An overview of causes and treatment options. Br J Nurs 2016;25:S35-40.  Back to cited text no. 4
    
5.
Juul A, Almstrup K, Andersson AM, Jensen TK, Jørgensen N, Main KM, et al. Possible fetal determinants of male infertility. Nat Rev Endocrinol 2014;10:553-62.  Back to cited text no. 5
    
6.
Travison TG, Morley JE, Araujo AB, O'Donnell AB, McKinlay JB. The relationship between libido and testosterone levels in aging men. J Clin Endocrinol Metab 2006;91:2509-13.  Back to cited text no. 6
    
7.
Keskin MZ, Budak S, Zeyrek T, Çelik O, Mertoglu O, Yoldas M, et al. The relationship between serum hormone levels (follicle-stimulating hormone, luteinizing hormone, total testosterone) and semen parameters. Arch Ital Urol Androl 2015;87:194-7.  Back to cited text no. 7
    
8.
Pavlovich CP, King P, Goldstein M, Schlegel PN. Evidence of a treatable endocrinopathy in infertile men. J Urol 2001;165:837-41.  Back to cited text no. 8
    
9.
Schlegel PN. Aromatase inhibitors for male infertility. Fertil Steril 2012;98:1359-62.  Back to cited text no. 9
    
10.
Chin KY, Ima-Nirwana S, Mohamed IN, Aminuddin A, Ngah WZ. Total testosterone and sex hormone-binding globulin are significantly associated with metabolic syndrome in middle-aged and elderly men. Exp Clin Endocrinol Diabetes 2013;121:407-12.  Back to cited text no. 10
    
11.
Salam R, Kshetrimayum AS, Keisam R. Testosterone and metabolic syndrome: The link. Indian J Endocrinol Metab 2012;16 Suppl 1:S12-9.  Back to cited text no. 11
    
12.
Macdonald AA, Stewart AW, Farquhar CM. Body mass index in relation to semen quality and reproductive hormones in New Zealand men: A cross-sectional study in fertility clinics. Hum Reprod 2013;28:3178-87.  Back to cited text no. 12
    
13.
Ho CH, Yu HJ, Wang CY, Jaw FS, Hsieh JT, Liao WC, et al. Prediabetes is associated with an increased risk of testosterone deficiency, independent of obesity and metabolic syndrome. PLoS One 2013;8:e74173.  Back to cited text no. 13
    
14.
Liu CC, Wu WJ, Lee YC, Wang CJ, Ke HL, Li WM, et al. The prevalence of and risk factors for androgen deficiency in aging Taiwanese men. J Sex Med 2009;6:936-46.  Back to cited text no. 14
    
15.
Glass AR, Swerdloff RS, Bray GA, Dahms WT, Atkinson RL. Low serum testosterone and sex-hormone-binding-globulin in massively obese men. J Clin Endocrinol Metab 1977;45:1211-9.  Back to cited text no. 15
    
16.
Cao J, Chen TM, Hao WJ, Li J, Liu L, Zhu BP, et al. Correlation between sex hormone levels and obesity in the elderly male. Aging Male 2012;15:85-9.  Back to cited text no. 16
    
17.
Allan CA, Strauss BJ, Burger HG, Forbes EA, McLachlan RI. The association between obesity and the diagnosis of androgen deficiency in symptomatic ageing men. Med J Aust 2006;185:424-7.  Back to cited text no. 17
    
18.
Shi MD, Chao JK, Ma MC, Hao LJ, Chao IC. Factors associated with sex hormones and erectile dysfunction in male Taiwanese participants with obesity. J Sex Med 2014;11:230-9.  Back to cited text no. 18
    
19.
McInnes KJ, Smith LB, Hunger NI, Saunders PT, Andrew R, Walker BR, et al. Deletion of the androgen receptor in adipose tissue in male mice elevates retinol binding protein 4 and reveals independent effects on visceral fat mass and on glucose homeostasis. Diabetes 2012;61:1072-81.  Back to cited text no. 19
    
20.
Santosa S, Jensen MD. Effects of male hypogonadism on regional adipose tissue fatty acid storage and lipogenic proteins. PLoS One 2012;7:e31473.  Back to cited text no. 20
    
21.
Kelly DM, Akhtar S, Sellers DJ, Muraleedharan V, Channer KS, Jones TH, et al. Testosterone differentially regulates targets of lipid and glucose metabolism in liver, muscle and adipose tissues of the testicular feminised mouse. Endocrine 2016;54:504-15.  Back to cited text no. 21
    
22.
Yuki A, Otsuka R, Kozakai R, Kitamura I, Okura T, Ando F, et al. Relationship between low free testosterone levels and loss of muscle mass. Sci Rep 2013;3:1818.  Back to cited text no. 22
    
23.
Cohen PG. The hypogonadal-obesity cycle: Role of aromatase in modulating the testosterone-estradiol shunt – A major factor in the genesis of morbid obesity. Med Hypotheses 1999;52:49-51.  Back to cited text no. 23
    
24.
Svartberg J, Agledahl I, Figenschau Y, Sildnes T, Waterloo K, Jorde R, et al. Testosterone treatment in elderly men with subnormal testosterone levels improves body composition and BMD in the hip. Int J Impot Res 2008;20:378-87.  Back to cited text no. 24
    
25.
Dimopoulou C, Ceausu I, Depypere H, Lambrinoudaki I, Mueck A, Pérez-López FR, et al. EMAS position statement: Testosterone replacement therapy in the aging male↰. Maturitas 2016;84:94-9.  Back to cited text no. 25
    
26.
Magnussen LV, Glintborg D, Hermann P, Hougaard DM, Højlund K, Andersen M, et al. Effect of testosterone on insulin sensitivity, oxidative metabolism and body composition in aging men with type 2 diabetes on metformin monotherapy. Diabetes Obes Metab 2016;18:980-9.  Back to cited text no. 26
    
27.
Bang JK, Lim JJ, Choi J, Won HJ, Yoon TK, Hong JY, et al. Reversible infertility associated with testosterone therapy for symptomatic hypogonadism in infertile couple. Yonsei Med J 2013;54:702-6.  Back to cited text no. 27
    
28.
Samplaski MK, Loai Y, Wong K, Lo KC, Grober ED, Jarvi KA, et al. Testosterone use in the male infertility population: Prescribing patterns and effects on semen and hormonal parameters. Fertil Steril 2014;101:64-9.  Back to cited text no. 28
    
29.
Jarow JP, Zirkin BR. The androgen microenvironment of the human testis and hormonal control of spermatogenesis. Ann N Y Acad Sci 2005;1061:208-20.  Back to cited text no. 29
    
30.
Schulster M, Bernie AM, Ramasamy R. The role of estradiol in male reproductive function. Asian J Androl 2016;18:435-40.  Back to cited text no. 30
[PUBMED]  [Full text]  
31.
Di Luigi L, Romanelli F, Sgrò P, Lenzi A. Andrological aspects of physical exercise and sport medicine. Endocrine 2012;42:278-84.  Back to cited text no. 31
    
32.
Vingren JL, Kraemer WJ, Ratamess NA, Anderson JM, Volek JS, Maresh CM, et al. Testosterone physiology in resistance exercise and training: The up-stream regulatory elements. Sports Med 2010;40:1037-53.  Back to cited text no. 32
    
33.
Ponholzer A, Plas E, Schatzl G, Struhal G, Brössner C, Mock K, et al. Relationship between testosterone serum levels and lifestyle in aging men. Aging Male 2005;8:190-3.  Back to cited text no. 33
    
34.
Svartberg J, Midtby M, Bønaa KH, Sundsfjord J, Joakimsen RM, Jorde R, et al. The associations of age, lifestyle factors and chronic disease with testosterone in men: The Tromsø study. Eur J Endocrinol 2003;149:145-52.  Back to cited text no. 34
    
35.
Osadchuk LV, Popova AV, Erkovich AA, Voroshilova NA, Osadchuk AV. Effects of smoking and alcohol consumption on reproductive and metabolic indicators in young men in Western Siberia. Urologiia 2017;(4):62-7.  Back to cited text no. 35
    
36.
Kirbas G, Abakay A, Topcu F, Kaplan A, Ünlu M, Peker Y. Obstructive sleep apnoea, cigarette smoking and serum testosterone levels in a male sleep clinic cohort. J Int Med Res 2007;35:38-45.  Back to cited text no. 36
    


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