The European Academy of Andrology (EAA) ultrasound study on healthy, fertile men: clinical, seminal and biochemical characteristics.
and metabolic parameters
clinical
fertile men
healthy
hormonal
male genital tract ultrasound
seminal parameters
sperm vitality
time to pregnancy
Journal
Andrology
ISSN: 2047-2927
Titre abrégé: Andrology
Pays: England
ID NLM: 101585129
Informations de publication
Date de publication:
09 2020
09 2020
Historique:
received:
20
03
2020
revised:
16
04
2020
accepted:
27
04
2020
pubmed:
1
5
2020
medline:
28
7
2021
entrez:
1
5
2020
Statut:
ppublish
Résumé
Infertility affects 7%-12% of men, and its etiology is unknown in half of cases. To fill this gap, use of the male genital tract color-Doppler ultrasound (MGT-CDUS) has progressively expanded. However, MGT-CDUS still suffers from lack of standardization. Hence, the European Academy of Andrology (EAA) has promoted a multicenter study ("EAA ultrasound study") to assess MGT-CDUS characteristics of healthy, fertile men to obtain normative parameters. To report (a) the development and methodology of the "EAA ultrasound study," (b) the clinical characteristics of the cohort of healthy, fertile men, and (c) the correlations of both fertility history and seminal features with clinical parameters. A cohort of 248 healthy, fertile men (35.3 ± 5.9 years) was studied. All subjects were asked to undergo, within the same day, clinical, biochemical, and seminal evaluation and MGT-CDUS before and after ejaculation. The clinical, seminal, and biochemical characteristics of the cohort have been reported here. The seminal characteristics were consistent with those reported by the WHO (2010) for the 50th and 5th centiles for fertile men. Normozoospermia was observed in 79.6% of men, while normal sperm vitality was present in almost the entire sample. Time to pregnancy (TTP) was 3.0[1.0-6.0] months. TTP was negatively correlated with sperm vitality (Adj.r =-.310, P = .011), but not with other seminal, clinical, or biochemical parameters. Sperm vitality and normal morphology were positively associated with fT3 and fT4 levels, respectively (Adj.r = .244, P < .05 and Adj.r = .232, P = .002). Sperm concentration and total count were negatively associated with FSH levels and positively, along with progressive motility, with mean testis volume (TV). Mean TV was 20.4 ± 4.0 mL, and the lower reference values for right and left testes were 15.0 and 14.0 mL. Mean TV was negatively associated with gonadotropin levels and pulse pressure. Varicocoele was found in 33% of men. The cohort studied confirms the WHO data for all semen parameters and represents a reference with which to assess MGT-CDUS normative parameters.
Sections du résumé
BACKGROUND
Infertility affects 7%-12% of men, and its etiology is unknown in half of cases. To fill this gap, use of the male genital tract color-Doppler ultrasound (MGT-CDUS) has progressively expanded. However, MGT-CDUS still suffers from lack of standardization. Hence, the European Academy of Andrology (EAA) has promoted a multicenter study ("EAA ultrasound study") to assess MGT-CDUS characteristics of healthy, fertile men to obtain normative parameters.
OBJECTIVES
To report (a) the development and methodology of the "EAA ultrasound study," (b) the clinical characteristics of the cohort of healthy, fertile men, and (c) the correlations of both fertility history and seminal features with clinical parameters.
METHODS
A cohort of 248 healthy, fertile men (35.3 ± 5.9 years) was studied. All subjects were asked to undergo, within the same day, clinical, biochemical, and seminal evaluation and MGT-CDUS before and after ejaculation.
RESULTS
The clinical, seminal, and biochemical characteristics of the cohort have been reported here. The seminal characteristics were consistent with those reported by the WHO (2010) for the 50th and 5th centiles for fertile men. Normozoospermia was observed in 79.6% of men, while normal sperm vitality was present in almost the entire sample. Time to pregnancy (TTP) was 3.0[1.0-6.0] months. TTP was negatively correlated with sperm vitality (Adj.r =-.310, P = .011), but not with other seminal, clinical, or biochemical parameters. Sperm vitality and normal morphology were positively associated with fT3 and fT4 levels, respectively (Adj.r = .244, P < .05 and Adj.r = .232, P = .002). Sperm concentration and total count were negatively associated with FSH levels and positively, along with progressive motility, with mean testis volume (TV). Mean TV was 20.4 ± 4.0 mL, and the lower reference values for right and left testes were 15.0 and 14.0 mL. Mean TV was negatively associated with gonadotropin levels and pulse pressure. Varicocoele was found in 33% of men.
CONCLUSIONS
The cohort studied confirms the WHO data for all semen parameters and represents a reference with which to assess MGT-CDUS normative parameters.
Types de publication
Journal Article
Multicenter Study
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1005-1020Informations de copyright
© 2020 American Society of Andrology and European Academy of Andrology.
Références
Krausz C. Male infertility: pathogenesis and clinical diagnosis. Best Pract Res Clin Endocrinol Metab. 2011;25:271-285.
Punab M, Poolamets O, Paju P, et al. Causes of male infertility: a 9-year prospective monocentre study on 1737 patients with reduced total sperm counts. Hum Reprod. 2017;32:18-31.
Lotti F, Maggi M. Sexual dysfunction and male infertility. Nat Rev Urol. 2018;15:287-307.
Dimitriadis F, Adonakis G, Kaponis A, Mamoulakis C, Takenaka A, Sofikitis N.Pre-testicular, testicular, and post-testicular causes of male infertility. In: Simoni M, Huhtaniemi IT eds. Endocrinology of the Testis and Male Reproduction, 1st edn. Chapter 32. Cham, Switzerland: Springer International Publishing AG; 2017:981-1028.
Lotti F, Maggi M. Ultrasound of the male genital tract in relation to male reproductive health. Hum Reprod Update. 2015;21:56-83.
Lotti F, Corona G, Cocci A, et al. The prevalence of midline prostatic cysts and the relationship between cyst size and semen parameters among infertile and fertile men. Hum Reprod. 2018;33:2023-2034.
World Health Organization. WHO Laboratory Manual for the Examination and Processing of Human Semen, 5th edn. Geneva, Switzerland: WHO Press; 2010.
Mínguez-Alarcón L, Williams PL, Chiu Y-H, et al. Secular trends in semen parameters among men attending a fertility center between 2000 and 2017: Identifying potential predictors. Environ Int. 2018;121:1297-1303.
Elbardisi H, Majzoub A, Al Said S, et al. Geographical differences in semen characteristics of 13 892 infertile men. Arab J Urol. 2018;16:3-9.
Khandwala YS, Zhang CA, Li S, Behr B, Guo D, Eisenberg ML. Racial variation in semen quality at fertility evaluation. Urology. 2017;106:96-102.
Li WN, Jia MM, Peng YQ, Ding R, Fan LQ, Liu G. Semen quality pattern and age threshold: a retrospective cross-sectional study of 71,623 infertile men in China, between 2011 and 2017. Reprod Biol Endocrinol. 2019;17:107.
Tuttelmann F, Nieschlag E. Classification of andrological disorders. In: Nieschlag E, Behre HM, Nieschlag S (eds). Andrology. Male Reproductive Health and Dysfunction, 3rd edn, Chapter 4. Berlin: Springer, 2010:87-92.
Ferlin A, Garolla A, Ghezzi M, Selice R, Palego P, Caretta N, Di Mambro A, Valente U, De Rocco Ponce M, Dipresa S, Sartori L, Plebani M, Foresta C. Sperm count and hypogonadism as markers of general male health. Eur Urol Focus. 2019 Aug 16. pii: S2405-4569(19)30210-X. doi: 10.1016/j.euf.2019.08.001. [Epub ahead of print]. PubMed PMID: 31427194.
Tang YG, Tang LX, Wang QL, et al. The reference values for semen parameters of 1213 fertile men in Guangdong Province in China. Asian J Androl. 2015;17:298-303.
Iwamoto T, Nozawa S, Yoshiike M, et al. Semen quality of fertile Japanese men: a cross-sectional population-based study of 792 men. BMJ Open. 2013;3(1):e002223.
Redmon JB, Thomas W, Ma W, et al. Semen parameters in fertile US men: the Study for Future Families. Andrology. 2013;1:806-814.
Ji H, Miao M, Liang H, et al. Exposure of environmental Bisphenol A in relation to routine sperm parameters and sperm movement characteristics among fertile men. Sci Rep. 2018;8:17548.
Yang B, Sun H, Wan Y, et al. Associations between testosterone, bone mineral density, vitamin D and semen quality in fertile and infertile Chinese men. Int J Androl. 2012;35:783-792.
Hofny ERM, Ali ME, Abdel-Hafez HZ, et al. Semen parameters and hormonal profile in obese fertile and infertile males. Fertil Steril. 2010;94:581-584.
Lotti F, Baldi E, Corona G, et al. Epididymal more than testicular abnormalities are associated with the occurrence of antisperm antibodies as evaluated by the MAR test. Hum Reprod. 2018;33:1417-1429.
Lotti F, Corona G, Castellini G, et al. Semen quality impairment is associated with sexual dysfunction according to its severity. Hum Reprod. 2016;31:2668-2680.
Grigorova M, Punab M, Poolamets O, Adler M, Vihljajev V, Laan M. Genetics of sex hormone-binding globulin and testosterone levels in fertile and infertile men of reproductive age. J Endocr Soc. 2017;1:560-576.
European Academy of Andrology. EAA Multicentre Study “Standardization of the male genital tract colour-Doppler ultrasound parameters in healthy, fertile men” http://www.andrologyacademy.net/studies. Accessed March 9, 2020.
Clinical and Laboratory Standard Institute (CLSI) Guidelines C28-A2. How to define and determine reference interval in the clinical laboratory: approved guideline -, 2nd edition. Wayne, PA, USA; 2000. Chapter 7.Analysis of Reference Values, pp. 13-14.
Regan L, Rai R. Epidemiology and the medical causes of miscarriage. Baillieres Best Pract Res Clin Obstet Gynaecol. 2000;14:839-854.
Royal College of Obstetrician and Gynaecologist. The investigation and treatment of couples with recurrent first-trimester and second-trimester miscarriage. London. 2011.
Baird DD, Wilcox AJ, Weinberg CR. Use of time to pregnancy to study environmental exposures. Am J Epidemiol. 1986;124:470-480.
Slama R, Eustache F, Ducot B, et al. Time to pregnancy and semen parameters: a cross-sectional study among fertile couples from four European cities. Hum Reprod. 2002;17:503-515.
Lombardo F, Pallotti F, Carngelutti F, Lenzi A. Anamnesis and physical examination. In: Simoni M, Huhtaniemi IT eds. Endocrinology of the Testis and Male Reproduction, 1st edn, Chapter 15. Cham, Switzerland: Springer International Publishing AG; 2017:481-494.
Colpi GM, Francavilla S, Haidl G, et al. European Academy of Andrology guideline Management of oligo-astheno-teratozoospermia. Andrology. 2018;6:513-524.
Rastrelli G, Corona G, Lotti F, Boddi V, Mannucci E, Maggi M. Relationship of testis size and LH levels with incidence of major adverse cardiovascular events in older men with sexual dysfunction. J Sex Med. 2013;10:2761-2773.
World Health Organization. Obesity: preventing and managing the global epidemic. Geneva. 2000.
Whelton PK, Carey RM, Aronow WS, et al. 2017 ACC/AHA/AAPA/ABC/ACPM/AGS/APhA/ASH/ASPC/NMA/PCNA Guideline for the Prevention, Detection, Evaluation, and Management of High Blood Pressure in Adults: Executive Summary: A Report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines. Circulation. 2018;138:e426-e483.
Lotti F, Corona G, Vitale P, et al. Current smoking is associated with lower seminal vesicles and ejaculate volume, despite higher testosterone levels, in male subjects of infertile couples. Hum Reprod. 2015;30:590-602.
Vermeulen A, Verdonck L, Kaufman JM. A critical evaluation of simple methods for the estimation of free testosterone in serum. J Clin Endocrinol Metab. 1999;84:3666-3672.
Simoni M, Santi D, Negri L, et al. Treatment with human, recombinant FSH improves sperm DNA fragmentation in idiopathic infertile men depending on the FSH receptor polymorphism p. N680S: a pharmacogenetic study. Hum Reprod. 2016;31:1960-1969.
Casamonti E, Vinci S, Serra E, et al. Short-term FSH treatment and sperm maturation: a prospective study in idiopathic infertile men. Andrology. 2017;5:414-422.
Tajar A, Forti G, O'Neill TW, et al. Characteristics of secondary, primary, and compensated hypogonadism in aging men: evidence from the European Male Ageing Study. J Clin Endocrinol Metab. 2010;95:1810-1818.
Maggi M, Buvat J, Corona G, Guay A, Torres LO. Hormonal causes of male sexual dysfunctions and their management (hyperprolactinemia, thyroid disorders, GH disorders, and DHEA). J Sex Med. 2013;10:661-677.
Lotti F, Corona G, Maseroli E, et al. Clinical implications of measuring prolactin levels in males of infertile couples. Andrology. 2013;1:764-771.
Gharib H, Tuttle RM, Baskin HJ, Fish LH, Singer PA, McDermott MT. Subclinical thyroid dysfunction: a joint statement on management from the American Association of Clinical Endocrinologists, the American Thyroid Association, and the Endocrine Society. J Clin Endocrinol Metab. 2005;90:581-585.
Lotti F, Maseroli E, Fralassi N, et al. Is thyroid hormones evaluation of clinical value in the work-up of males of infertile couples? Hum Reprod. 2016;31:518-529.
Alberti KG, Eckel RH, Grundy SM, et al. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation. 2009;120:1640-1645.
Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults. Executive Summary of the Third Report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III). JAMA. 2001;285(19):2486-2497.
Bhasin S, Brito JP, Cunningham GR, et al. Testosterone therapy in men with hypogonadism: an endocrine society clinical practice guideline. J Clin Endocrinol Metab. 2018;1(103):1715-1744.
Wang C, Nieschlag E, Swerdloff R, et al. Investigation, treatment, and monitoring of late-onset hypogonadism in males: ISA, ISSAM, EAU, EAA, and ASA recommendations. J Androl. 2009;30:1-9.
American College of Obstetricians and Gynecologists Committee on Gynecologic Practice and Practice Committee. Female age-related fertility decline. Committee Opinion No. 589. Fertil Steril. 2014;101:633-634.
Baird DT, Collins J, Egozcue J, et al. ESHRE Capri Workshop Group. Fertility and ageing. Hum Reprod Update. 2005;11:261-276.
Rowe PJ, Comhaire FH, Hargreave TB, Mahmoud AM, World Health Organization. WHO Manual for the Standardized Investigation, Diagnosis, and Management of the Infertile Male. Bath, UK: Cambridge University Press; 2000.
Pilatz A, Discher T, Lochnit G, et al. Semen quality in HIV patients under stable antiretroviral therapy is impaired compared to WHO 2010 reference values and on sperm proteome level. AIDS. 2014;28:875-880.
Evgeni E, Lymberopoulos G, Gazouli M, Asimakopoulos B. Conventional semen parameters and DNA fragmentation in relation to fertility status in a Greek population. Eur J Obstet Gynecol Reprod Biol. 2015;188:17-23.
Savasi V, Parisi F, Oneta M, et al. Effects of highly active antiretroviral therapy on semen parameters of a cohort of 770 HIV-1 infected men. PLoS ONE. 2019;14:e0212194.
Rowe PJ, Comhaire FH, Hargreave TB, Heather J, Mellows; World Health Organization. WHO Manual for the Standardized Investigation and Diagnosis of the Infertile Couple. Cambridge: Cambridge University Press; 1993.
Zegers-Hochschild F, Adamson GD, Dyer S, et al. The International Glossary on Infertility and Fertility Care, 2017. Fertil Steril. 2017;108:393-406.
National Institute for Health and Clinical Excellence (NICE) guidelines. Fertility Assessment and Treatment for People with Fertility Problems. London: RCOG Press; 2004.
te Velde ER, Eijkemans R, Habbema HD. Variation in couple fecundity and time to pregnancy, an essential concept in human reproduction. Lancet. 2000;355:1928-1929.
Andersen AG, Ziebe S, Jørgensen N, Petersen JH, Skakkebaek NE, Andersen AN. Time to pregnancy in relation to semen quality assessed by CASA before and after sperm separation. Hum Reprod. 2002;17:173-177.
Vander Borght M, Wyns C. Fertility and infertility: Definition and epidemiology. Clin Biochem. 2018;62:2-10.
Moskovtsev SI, Librach CL. Methods of sperm vitality assessment. Methods Mol Biol. 2013;927:13-19.
Samplaski MK, Dimitromanolakis A, Lo KC, et al. The relationship between sperm viability and DNA fragmentation rates. Reprod Biol Endocrinol. 2015;13:42.
Shen HM, Dai J, Chia SE, Lim A, Ong CN. Detection of apoptotic alterations in sperm in subfertile patients and their correlations with sperm quality. Hum Reprod. 2002;17:1266-1273.
Cohen-Bacrie P, Belloc S, Ménézo YJ, Clement P, Hamidi J, Benkhalifa M. Correlation between DNA damage and sperm parameters: a prospective study of 1,633 patients. Fertil Steril. 2009;91:1801-1805.
Brahem S, Mehdi M, Landolsi H, Mougou S, Elghezal H, Saad A. Semen parameters and sperm DNA fragmentation as causes of recurrent pregnancy loss. Urology. 2011;78:792-796.
Bonde JP, Ernst E, Jensen TK, et al. Relation between semen quality and fertility: a population-based study of 430 first-pregnancy planners. Lancet. 1998;352:1172-1177.
Zinaman MJ, Brown CC, Selevan SG, Clegg ED. Semen quality and human fertility: a prospective study with healthy couples. J Androl. 2000;21:145-153.
Buck Louis GM, Sundaram R, Schisterman EF, et al. Semen quality and time to pregnancy: the Longitudinal Investigation of Fertility and the Environment Study. Fertil Steril. 2014;101:453-462.
Du Plessis SS, Gokul S, Agarwal A. Semen hyperviscosity: causes, consequences, and cures. Front Biosci (Elite Ed). 2013;5:224-231.
Agarwal A, Gupta S, Du Plessis S, et al. Abstinence time and its impact on basic and advanced semen parameters. Urology. 2016;94:102-110.
Stanford JB, Dunson DB. Effects of sexual intercourse patterns in time to pregnancy studies. Am J Epidemiol. 2007;165:1088-1095.
Hornstein MD, Gibbons WE, Shenken RS.Optimizing natural fertility in couples planning pregnancy. https://www.uptodate.com/contents/optimizing-natural-fertility-in-couples-planning-pregnancy. Accessed November 11, 2019.
Hunault CC, Habbema JD, Eijkemans MJ, Collins JA, Evers JL, te Velde ER. Two new prediction rules for spontaneous pregnancy leading to live birth among subfertile couples, based on the synthesis of three previous models. Hum Reprod. 2004;19:2019-2026.
Sedgh G, Bearak J, Singh S, et al. Abortion incidence between 1990 and 2014: global, regional, and subregional levels and trends. Lancet. 2016;388:258-267.
Mäkelä JA, Toppari J.Spermatogenesis. In: Simoni M, Huhtaniemi IT eds. Endocrinology of the Testis and Male Reproduction, 1st edn, Chapter 13. Cham, Switzerland: Springer International Publishing AG; 2017:417-456.
Rajender S, Monica MG, Walter L, Agarwal A. Thyroid, spermatogenesis, and male infertility. Front Biosci (Elite Ed). 2011;3:843-855.
De Paul AL, Mukdsi JH, Pellizas CG, et al. Thyroid hormone receptor alpha 1-beta 1 expression in epididymal epithelium from euthyroid and hypothyroid rats. Histochem Cell Biol. 2008;129:631-642.
Carosa E, Di Sante S, Rossi S, et al. Ontogenetic profile of the expression of thyroid hormone receptors in rat and human corpora cavernosa of the penis. J Sex Med. 2010;7:1381-1390.
La Vignera S, Vita R. Thyroid dysfunction and semen quality. Int J Immunopathol Pharmacol. 2018;32:2058738418775241.
Corrales Hernández JJ, Miralles García JM, García Diez LC. Primary hypothyroidism and human spermatogenesis. Arch Androl. 1990;25:21-27.
Krassas GE, Papadopoulou F, Tziomalos K, Zeginiadou T, Pontikides N. Hypothyroidism has an adverse effect on human spermatogenesis: a prospective, controlled study. Thyroid. 2008;18:1255-1259.
Condorelli RA, La Vignera S, Mongioì LM, et al. Thyroid Hormones and Spermatozoa:in vitro effects on Sperm Mitocondria, Viability and DNA Integrity. J Clin Med. 2019;8:756.
Rastrelli G, Lotti F, Reisman Y, Sforza A, Maggi M, Corona G. Metabolically healthy and unhealthy obesity in erectile dysfunction and male infertility. Expert Rev Endocrinol Metab. 2019;14:321-334.
Cazzaniga W, Capogrosso P, Ventimiglia E, et al. High blood pressure is a highly prevalent but unrecognised condition in primary infertile men: results of a cross-sectional study. Eur Urol Focus. 2020;6:178-183.
Muciaccia B, Pensini S, Culasso F, et al. Higher clusterin immunolabeling and sperm DNA damage levels in hypertensive men compared with controls. Hum Reprod. 2012;27:2267-2276.
Lotti F, Corona G, Degli Innocenti S, et al. Seminal, ultrasound and psychobiological parameters correlate with metabolic syndrome in male members of infertile couples. Andrology. 2013;1:229-239.
Mbah AU, Ndukwu GO, Ghasi SI, et al. Low-dose lisinopril in normotensive men with idiopathic oligospermia and infertility: a 5-year randomized, controlled, crossover pilot study. Clin Pharmacol Ther. 2012;91:582-589.
Kwok MK, Leung GM, Schooling CM. Pubertal testis volume, age at pubertal onset, and adolescent blood pressure: Evidence from Hong Kong's "Children of 1997" birth cohort. Am J Hum Biol. 2017;29.
Jørgensen N, Carlsen E, Nermoen I, et al. East-West gradient in semen quality in the Nordic-Baltic area: a study of men from the general population in Denmark, Norway, Estonia and Finland. Hum Reprod. 2002;17:2199-2208.
Sakamoto H, Ogawa Y, Yoshida H. Relationship between testicular volume and testicular function: comparison of the Prader orchidometric and ultrasonographic measurements in patients with infertility. Asian J Androl. 2008;10:319-324.
Ruiz-Olvera SF, Rajmil O, Sanchez-Curbelo JR, Vinay J, Rodriguez-Espinosa J, Ruiz-Castañé E. Association of serum testosterone levels and testicular volume in adult patients. Andrologia. 2018;50(3):e12933.
Jensen TK, Jørgensen N, Punab M, et al. Association of in utero exposure to maternal smoking with reduced semen quality and testis size in adulthood: a cross-sectional study of 1,770 young men from the general population in five European countries. Am J Epidemiol. 2004;159:49-58.
Takihara H, Cosentino MJ, Sakatoku J, Cockett AT. Significance of testicular size measurement in andrology: II. Correlation of testicular size with testicular function. J Urol. 1987;137:416-419.
Forti G, Krausz C. Clinical review 100: Evaluation and treatment of the infertile couple. J Clin Endocrinol Metab. 1998;83:4177-4188.
Freeman S, Bertolotto M, Richenberg J, et al. Ultrasound evaluation of varicoceles: guidelines and recommendations of the European Society of Urogenital Radiology Scrotal and Penile Imaging Working Group (ESUR-SPIWG) for detection, classification, and grading. Eur Radiol. 2020;30:11-25.
Practice Committee of American Society for Reproductive Medicine. Report on varicocele and infertility. Fertil Steril. 2008;90:S247-249.
Jungwirth A, Diemer T, Kopa Z, Krausz C, Minhas S, Tournaye H.Guidelines on Male Infertility, European Association of Urology Guidelines. https://uroweb.org/guideline/male-infertility/ Accessed March 9, 2020.
Christensen JD, Dogra VS. The undescended testis. Semin Ultrasound CT MR. 2007;28:307-316.
Pilatz A, Wagenlehner F, Bschleipfer T, et al. Acute epididymitis in ultrasound: results of a prospective study with baseline and follow-up investigations in 134 patients. Eur J Radiol. 2013;82:e762-768.
Rusz A, Pilatz A, Wagenlehner F, et al. Influence of urogenital infections and inflammation on semen quality and male fertility. World J Urol. 2012;30:23-30.
Pasqualotto FF, Sobreiro BP, Hallak J, Pasqualotto EB, Lucon AM. Cigarette smoking is related to a decrease in semen volume in a population of fertile men. BJU Int. 2006;97:324-326.
Ehala-Aleksejev K, Punab M. The effect of metabolic syndrome on male reproductive health: A cross-sectional study in a group of fertile men and male partners of infertile couples. PLoS ONE. 2018;13:e0194395.
Tang Q, Pan F, Wu X, et al. Semen quality and cigarette smoking in a cohort of healthy fertile men. Environ Epidemiol. 2019;3:e055.
WHO. Global report on trends in prevalence of tobacco smoking 2000-2025, second edition. Geneva: World Health Organization; 2018.
Sharma R, Harlev A, Agarwal A, Esteves SC. Cigarette Smoking and Semen Quality: A New Meta-analysis Examining the Effect of the 2010 World Health Organization Laboratory Methods for the Examination of Human Semen. Eur Urol. 2016;70:635-645.
Practice Committee of the American Society for Reproductive Medicine. Practice Committee of the American Society for Reproductive Medicine. Smoking and infertility: a committee opinion. Fertil Steril. 2018;110:611-618.
Li Y, Lin H, Li Y, Cao J. Association between socio-psycho-behavioral factors and male semen quality: systematic review and meta-analyses. Fertil Steril. 2011;95:116-123.
Ricci E, Al Beitawi S, Cipriani S, et al. Semen quality and alcohol intake: a systematic review and meta-analysis. Reprod Biomed Online. 2017;34:38-47.
Jensen TK, Swan S, Jørgensen N, et al. Alcohol and male reproductive health: a cross-sectional study of 8344 healthy men from Europe and the USA. Hum Reprod. 2014;29:1801-1809.
European Monitoring Center for Drug and Drug Addiction. http://www.emcdda.europa.eu/data/stats2019/gps. Accessed March 9, 2020.
Rajanahally S, Raheem O, Rogers M, et al. The relationship between cannabis and male infertility, sexual health, and neoplasm: a systematic review. Andrology. 2019;7:139-147.
Payne KS, Mazur DJ, Hotaling JM, Pastuszak AW. Cannabis and Male Fertility: A Systematic Review. J Urol. 2019;202:674-681.
Bonde JP. Male reproductive organs are at risk from environmental hazards. Asian J Androl. 2010;12:152-156.
Eurostat. https://ec.europa.eu/eurostat/web/products-eurostat-news/-/DDN-20170302-1. Updated March 2, 2017. Accessed March 9, 2020.
Ibañez-Perez J, Santos-Zorrozua B, Lopez-Lopez E, Matorras R, Garcia-Orad A. An update on the implication of physical activity on semen quality: a systematic review and meta-analysis. Arch Gynecol Obstet. 2019;299:901-921.