Metabolic syndrome and smoking are independent risk factors of male idiopathic infertility

Charlotte Dupont, Céline Faure, Frederic Daoud, Benoit Gautier, Sébastien Czernichow, Rachel Lévy, ALIFERT collaborative group, Isabelle Aknin, Isabelle Cedrin-Durnerin, Steven Cens, Pascale Chavatte-Palmer, Serge Hercberg, Khaled Pocate, Nathalie Sermondade, Claude Uthurriague, Jean-Philippe Wolf, Charlotte Dupont, Céline Faure, Frederic Daoud, Benoit Gautier, Sébastien Czernichow, Rachel Lévy, ALIFERT collaborative group, Isabelle Aknin, Isabelle Cedrin-Durnerin, Steven Cens, Pascale Chavatte-Palmer, Serge Hercberg, Khaled Pocate, Nathalie Sermondade, Claude Uthurriague, Jean-Philippe Wolf

Abstract

Background: Overweight and obesity are known to impact male fertility and are commonly associated with abdominal obesity and metabolic disorders. The association between abdominal obesity or metabolic syndrome with male reproduction has not been fully investigated. Moreover, many factors may interfere with the evaluation of the impact of metabolic syndrome on male fertility. Thus, tobacco is known to alter the spermatic parameters and phenomena linking smoking with metabolic syndrome are therefore complex. The main objective of this study has been to investigate the potential association of metabolic syndrome with male idiopathic infertility given smoking status.

Materiel and methods: The data of this study concerned infertile (n = 96) and fertile (n = 100) men under 45 years of age who have been recruited in the ALIFERT case-control study. Body mass index and waist circumference were measured. Serum triglycerides, cholesterol (total, high density lipoprotein, and low density lipoprotein cholesterol) and fasting blood glucose were assayed. Metabolic syndrome has been diagnosed in the presence of at least three of the following criteria: increased waist circumference, high triglycerides, fasting glucose or arterial blood pressure and low high density lipoprotein cholesterol.

Results: The present study reports that infertile men are in poorer health condition compared to fertile men and are more often smokers. The results of this study suggested metabolic syndrome and smoking to be independent risk factor for idiopathic infertility.

Conclusions: Metabolic syndrome and smoking should systematically be checked at the beginning of medical care in infertile males and personal and multifaceted coaching should be proposed to deal jointly with smoking and metabolic disorders.

Trial registration: NCT01093378 ALIFERT. Registered: March 25, 2010.

Keywords: Male fertility; Metabolic syndrome; Smoking.

Conflict of interest statement

Competing interestsAll authors declare no competing financial interests and consent for publication.

References

    1. Levine H, Jorgensen N, Martino-Andrade A, et al. Temporal trends in sperm count: a systematic review and meta-regression analysis. Hum Reprod Update. 2017;23(6):646–659. doi: 10.1093/humupd/dmx022.
    1. Sharpe RM, Irvine DS. How strong is the evidence of a link between environmental chemicals and adverse effects on human reproductive health? BMJ. 2004;328(7437):447–451. doi: 10.1136/bmj.328.7437.447.
    1. Michalakis K, Mintziori G, Kaprara A, Tarlatzis BC, Goulis DG. The complex interaction between obesity, metabolic syndrome and reproductive axis: a narrative review. Metabolism. 2013;62(4):457–478. doi: 10.1016/j.metabol.2012.08.012.
    1. Faure C, Dupont C, Baraibar MA, et al. In subfertile couple, abdominal fat loss in men is associated with improvement of sperm quality and pregnancy: a case-series. PLoS One. 2014;9(2):e86300. doi: 10.1371/journal.pone.0086300.
    1. Ramlau-Hansen CH, Thulstrup AM, Nohr EA, Bonde JP, Sorensen TI, Olsen J. Subfecundity in overweight and obese couples. Hum Reprod. 2007;22(6):1634–1637. doi: 10.1093/humrep/dem035.
    1. Belloc S, Cohen-Bacrie M, Amar E, et al. High body mass index has a deleterious effect on semen parameters except morphology: results from a large cohort study. Fertil Steril. 2014;102(5):1268–1273. doi: 10.1016/j.fertnstert.2014.07.1212.
    1. Chavarro JE, Toth TL, Wright DL, Meeker JD, Hauser R. Body mass index in relation to semen quality, sperm DNA integrity, and serum reproductive hormone levels among men attending an infertility clinic. Fertil Steril. 2010;93(7):2222–2231. doi: 10.1016/j.fertnstert.2009.01.100.
    1. Kort HI, Massey JB, Elsner CW, et al. Impact of body mass index values on sperm quantity and quality. J Androl. 2006;27(3):450–452. doi: 10.2164/jandrol.05124.
    1. Sermondade N, Faure C, Fezeu L, et al. BMI in relation to sperm count: an updated systematic review and collaborative meta-analysis. Hum Reprod Update. 2013;19(3):221–231. doi: 10.1093/humupd/dms050.
    1. Dupont C, Faure C, Sermondade N, et al. Obesity leads to higher risk of sperm DNA damage in infertile patients. Asian J Androl. 2013;15(5):622–625. doi: 10.1038/aja.2013.65.
    1. Onat A, Avci GS, Barlan MM, Uyarel H, Uzunlar B, Sansoy V. Measures of abdominal obesity assessed for visceral adiposity and relation to coronary risk. Int J Obes Relat Metab Disord. 2004;28(8):1018–1025. doi: 10.1038/sj.ijo.0802695.
    1. 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(16):1640–1645. doi: 10.1161/CIRCULATIONAHA.109.192644.
    1. Leisegang K, Udodong A, Bouic PJ, Henkel RR. Effect of the metabolic syndrome on male reproductive function: a case-controlled pilot study. Andrologia. 2014;46(2):167–176. doi: 10.1111/and.12060.
    1. Ventimiglia E, Capogrosso P, Colicchia M, et al. Metabolic syndrome in white European men presenting for primary couple’s infertility: investigation of the clinical and reproductive burden. Andrology. 2016;4(5):944–951. doi: 10.1111/andr.12232.
    1. Lu JC, Jing J, Yao Q, et al. Relationship between lipids levels of serum and seminal plasma and semen parameters in 631 Chinese subfertile men. PLoS One. 2016;11(1):e0146304. doi: 10.1371/journal.pone.0146304.
    1. Leisegang K, Bouic PJ, Menkveld R, Henkel RR. Obesity is associated with increased seminal insulin and leptin alongside reduced fertility parameters in a controlled male cohort. Reprod Biol Endocrinol. 2014;12:34. doi: 10.1186/1477-7827-12-34.
    1. Pilatz A, Hudemann C, Wolf J, et al. Metabolic syndrome and the seminal cytokine network in morbidly obese males. Andrology. 2017;5(1):23–30. doi: 10.1111/andr.12296.
    1. Teo KK, Ounpuu S, Hawken S, et al. Tobacco use and risk of myocardial infarction in 52 countries in the INTERHEART study: a case-control study. Lancet. 2006;368(9536):647–658. doi: 10.1016/S0140-6736(06)69249-0.
    1. Oboni JB, Marques-Vidal P, Bastardot F, Vollenweider P, Waeber G. Impact of smoking on fertility and age of menopause: a population-based assessment. BMJ Open. 2016;6(11):e012015. doi: 10.1136/bmjopen-2016-012015.
    1. Sansone A, Di Dato C, de Angelis C, et al. Smoke, alcohol and drug addiction and male fertility. Reprod Biol Endocrinol. 2018;16(1):3. doi: 10.1186/s12958-018-0320-7.
    1. Ramlau-Hansen CH, Thulstrup AM, Aggerholm AS, Jensen MS, Toft G, Bonde JP. Is smoking a risk factor for decreased semen quality? A cross-sectional analysis. Hum Reprod. 2007;22(1):188–196. doi: 10.1093/humrep/del364.
    1. 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(4):635–645. doi: 10.1016/j.eururo.2016.04.010.
    1. Harlev A, Agarwal A, Gunes SO, Shetty A, du Plessis SS. Smoking and male infertility: an evidence-based review. World J Mens Health. 2015;33(3):143–160. doi: 10.5534/wjmh.2015.33.3.143.
    1. Krukowski RA, Bursac Z, Little MA, Klesges RC. The relationship between body mass index and post-cessation weight gain in the year after quitting smoking: a cross-sectional study. PLoS One. 2016;11(3):e0151290. doi: 10.1371/journal.pone.0151290.
    1. Aubin HJ, Farley A, Lycett D, Lahmek P, Aveyard P. Weight gain in smokers after quitting cigarettes: meta-analysis. BMJ. 2012;345:e4439. doi: 10.1136/bmj.e4439.
    1. Sun K, Liu J, Ning G. Active smoking and risk of metabolic syndrome: a meta-analysis of prospective studies. PLoS One. 2012;7(10):e47791. doi: 10.1371/journal.pone.0047791.
    1. Slagter SN, van Vliet-Ostaptchouk JV, Vonk JM, et al. Associations between smoking, components of metabolic syndrome and lipoprotein particle size. BMC Med. 2013;11:195. doi: 10.1186/1741-7015-11-195.
    1. Clair C, Chiolero A, Faeh D, et al. Dose-dependent positive association between cigarette smoking, abdominal obesity and body fat: cross-sectional data from a population-based survey. BMC Public Health. 2011;11:23. doi: 10.1186/1471-2458-11-23.
    1. de Oliveira Fontes Gasperin L, Neuberger M, Tichy A, Moshammer H. Cross-sectional association between cigarette smoking and abdominal obesity among Austrian bank employees. BMJ Open. 2014;4(7):e004899. doi: 10.1136/bmjopen-2014-004899.
    1. Faure C, Dupont C, Chavatte-Palmer P, Gautier B, Levy R, Group AC Are semen parameters related to birth weight? Fertil Steril. 2015;103(1):6–10. doi: 10.1016/j.fertnstert.2014.11.027.
    1. Ray A, Shah A, Gudi A, Homburg R. Unexplained infertility: an update and review of practice. Reprod BioMed Online. 2012;24(6):591–602. doi: 10.1016/j.rbmo.2012.02.021.
    1. Smith S, Pfeifer SM, Collins JA. Diagnosis and management of female infertility. JAMA. 2003;290(13):1767–1770. doi: 10.1001/jama.290.13.1767.
    1. Deveci SE, Deveci F, Acik Y, Ozan AT. The measurement of exhaled carbon monoxide in healthy smokers and non-smokers. Respir Med. 2004;98(6):551–556. doi: 10.1016/j.rmed.2003.11.018.
    1. Maga M, Janik MK, Wachsmann A, et al. Influence of air pollution on exhaled carbon monoxide levels in smokers and non-smokers. A prospective cross-sectional study. Environ Res. 2017;152:496–502. doi: 10.1016/j.envres.2016.09.004.
    1. La Vignera S, Condorelli RA, Vicari E, Calogero AE. Negative effect of increased body weight on sperm conventional and nonconventional flow cytometric sperm parameters. J Androl. 2012;33(1):53–58. doi: 10.2164/jandrol.110.012120.
    1. La Vignera S, Condorelli R, Vicari E, D'Agata R, Calogero AE. Diabetes mellitus and sperm parameters. J Androl. 2012;33(2):145–153. doi: 10.2164/jandrol.111.013193.
    1. Trummer H, Habermann H, Haas J, Pummer K. The impact of cigarette smoking on human semen parameters and hormones. Hum Reprod. 2002;17(6):1554–1559. doi: 10.1093/humrep/17.6.1554.
    1. 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(3):590–602. doi: 10.1093/humrep/deu347.
    1. Camacho EM, Huhtaniemi IT, O'Neill TW, et al. Age-associated changes in hypothalamic-pituitary-testicular function in middle-aged and older men are modified by weight change and lifestyle factors: longitudinal results from the European male ageing study. Eur J Endocrinol. 2013;168(3):445–455. doi: 10.1530/EJE-12-0890.
    1. Condorelli RA, La Vignera S, Giacone F, et al. In vitro effects of nicotine on sperm motility and bio-functional flow cytometry sperm parameters. Int J Immunopathol Pharmacol. 2013;26(3):739–746. doi: 10.1177/039463201302600317.
    1. Calogero A, Polosa R, Perdichizzi A, et al. Cigarette smoke extract immobilizes human spermatozoa and induces sperm apoptosis. Reprod BioMed Online. 2009;19(4):564–571. doi: 10.1016/j.rbmo.2009.05.004.
    1. Tian J, Venn A, Otahal P, Gall S. The association between quitting smoking and weight gain: a systemic review and meta-analysis of prospective cohort studies. Obes Rev. 2015;16(10):883–901. doi: 10.1111/obr.12304.
    1. Sperling LS, Mechanick JI, Neeland IJ, et al. The CardioMetabolic health Alliance: working toward a new care model for the metabolic syndrome. J Am Coll Cardiol. 2015;66(9):1050–1067. doi: 10.1016/j.jacc.2015.06.1328.
    1. Kaukua J, Pekkarinen T, Sane T, Mustajoki P. Sex hormones and sexual function in obese men losing weight. Obes Res. 2003;11(6):689–694. doi: 10.1038/oby.2003.98.
    1. Hakonsen LB, Thulstrup AM, Aggerholm AS, et al. Does weight loss improve semen quality and reproductive hormones? Results from a cohort of severely obese men. Reprod Health. 2011;8:24. doi: 10.1186/1742-4755-8-24.
    1. Hannan JL, Maio MT, Komolova M, Adams MA. Beneficial impact of exercise and obesity interventions on erectile function and its risk factors. J Sex Med. 2009;6(Suppl 3):254–261. doi: 10.1111/j.1743-6109.2008.01143.x.
    1. Rafiee B, Morowvat MH, Rahimi-Ghalati N. Comparing the effectiveness of dietary vitamin C and exercise interventions on fertility parameters in Normal obese men. Urol J. 2016;13(2):2635–2639.
    1. La Vignera S, Condorelli RA, Balercia G, Vicari E, Calogero AE. Does alcohol have any effect on male reproductive function? A review of literature. Asian J Androl. 2013;15(2):221–225. doi: 10.1038/aja.2012.118.
    1. La Vignera S, Condorelli RA, Vicari E, Calogero AE. Statins and erectile dysfunction: a critical summary of current evidence. J Androl. 2012;33(4):552–558. doi: 10.2164/jandrol.111.015230.
    1. La Vignera S, Condorelli RA, Vicari E, D'Agata R, Calogero AE. Effects of the exposure to mobile phones on male reproduction: a review of the literature. J Androl. 2012;33(3):350–356. doi: 10.2164/jandrol.111.014373.

Source: PubMed

스폰서 및 공동 작업자

건강 상태

약물 개입

3
구독하다