Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Effect of paternal smoking on pre-implantation embryonic development: a prospective cohort study

Jean Frappier A B , Aurélie Martinaud A B , Julie Barberet A B , Céline Bruno A B , Magali Guilleman A B , Céline Amblot C , Adrien Guilloteau D and Patricia Fauque https://orcid.org/0000-0002-9708-1710 A B *
+ Author Affiliations
- Author Affiliations

A Laboratoire de Biologie de la Reproduction, Hôpital François Mitterrand, Université de Bourgogne, 14 rue Gaffarel, 21079 Dijon CEDEX, France.

B INSERM UMR1231, Université de Bourgogne Franche comté, Dijon, France.

C Service de Gynécologie-Obstétrique, Hôpital François Mitterrand, Université de Bourgogne, Dijon, France.

D USMR, Dijon University Hospital, F-21000 Dijon, France.

* Correspondence to: patricia.fauque@chu-dijon.fr

Handling Editor: James Cummins

Reproduction, Fertility and Development 34(15) 971-979 https://doi.org/10.1071/RD22093
Published online: 29 August 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Context: Recent studies have failed to demonstrate the negative impact of male tobacco smoking on embryo development, raising the question of its actual implication on natural fecundity and assisted reproductive techniques outcomes.

Aims: To assess the impact of paternal smoking on embryo development.

Methods: In this prospective cohort study, 252 men from couples undergoing in vitro fertilisation (IVF) were included. Each patient was interviewed and took a carbon monoxide breath-test, creating three groups: non-smokers (n = 113), former smokers (n = 81) and active smokers (n = 58). The Top-grade embryo ratio (primary endpoint), embryo morphokinetic parameters and clinical outcomes were assessed.

Key results: In a multivariate analyses based on 1521 embryos, no significant difference was found in the top-grade embryo ratio between the groups. Tobacco smoking had no impact on clinical outcomes. Compared to non-smokers the time to the pronuclei fading (tPNf, P = 0.006) and the time to the first embryonic cleavage (t2, P = 0.002) were shorter in smokers, and the t2 was also slightly shorter in former smokers (P = 0.045). No other differences were found in the morphokinetic parameters.

Conclusion: Even if a few differences were observed in the first timing of embryonic events, this study did not highlight a major embryonic and clinical impact of the paternal smoking status.

Implication: The results obtained here are reassuring towards IVF outcomes. As maternal smoking is highly controlled in the IVF patients in this study, we speculate that the sperm selection process may limit the adverse effects of tobacco consumption on embryo development.

Keywords: assisted reproductive techniques, clinical outcomes, embryo morphokinetics, embryonic development, in vitro fertilisation, time-lapse imaging, tobacco smoking, top-grade embryo.


References

Albert M, Auger J, Eustache F (2009) ‘Exploration de la fonction de la reproduction versant masculin’. (Cahier de Formation Biologie médicale Ed Bioforma) 42 p.

Alpha Scientists in Reproductive Medicine and ESHRE Special Interest Group of Embryology (2011). The Istanbul consensus workshop on embryo assessment, proceedings of an expert meeting. Human Reproduction 26, 1270–1283.
The Istanbul consensus workshop on embryo assessment, proceedings of an expert meeting.Crossref | GoogleScholarGoogle Scholar |

Avidor-Reiss, T, Mazur, M, Fishman, EL, and Sindhwani, P (2019). The role of sperm centrioles in human reproduction – the known and the unknown. Frontiers in Cell and Developmental Biology 7, 188.
The role of sperm centrioles in human reproduction – the known and the unknown.Crossref | GoogleScholarGoogle Scholar |

Barberet, J, Chammas, J, Bruno, C, Valot, E, Vuillemin, C, Jonval, L, Choux, C, Sagot, P, Soudry, A, and Fauque, P (2018). Randomized controlled trial comparing embryo culture in two incubator systems: G185 K-System versus EmbryoScope. Fertility and Sterility 109, 302–309.e1.
Randomized controlled trial comparing embryo culture in two incubator systems: G185 K-System versus EmbryoScope.Crossref | GoogleScholarGoogle Scholar |

Barberet, J, Bruno, C, Valot, E, Antunes-Nunes, C, Jonval, L, Chammas, J, Choux, C, Ginod, P, Sagot, P, Soudry-Faure, A, and Fauque, P (2019). Can novel early non-invasive biomarkers of embryo quality be identified with time-lapse imaging to predict live birth? Human Reproduction 34, 1439–1449.
Can novel early non-invasive biomarkers of embryo quality be identified with time-lapse imaging to predict live birth?Crossref | GoogleScholarGoogle Scholar |

Bourdon, M, Ferreux, L, Maignien, C, Patrat, C, Marcellin, L, Pocate-Cheriet, K, Chapron, C, and Santulli, P (2020). Tobacco consumption is associated with slow-growing day-6 blastocysts. F&S Reports 1, 30–36.
Tobacco consumption is associated with slow-growing day-6 blastocysts.Crossref | GoogleScholarGoogle Scholar |

Bruno, C, Bourredjem, A, Barry, F, Frappier, J, Martinaud, A, Chamoy, B, Hance, I, Ginod, P, Cavalieri, M, Amblot, C, Binquet, C, Barberet, J, and Fauque, P (2022). Analysis and quantification of female and male contributions to the first stages of embryonic kinetics: study from a time-lapse system. Journal of Assisted Reproduction and Genetics 39, 85–95.
Analysis and quantification of female and male contributions to the first stages of embryonic kinetics: study from a time-lapse system.Crossref | GoogleScholarGoogle Scholar |

Budani, MC, Fensore, S, Di Marzio, M, and Tiboni, GM (2018). Cigarette smoking impairs clinical outcomes of assisted reproductive technologies: a meta-analysis of the literature. Reproductive Toxicology 80, 49–59.
Cigarette smoking impairs clinical outcomes of assisted reproductive technologies: a meta-analysis of the literature.Crossref | GoogleScholarGoogle Scholar |

Ciray, HN, Campbell, A, Agerholm, IE, Aguilar, J, Chamayou, S, Esbert, M, Sayed, S, Time-Lapse User Group (2014). Proposed guidelines on the nomenclature and annotation of dynamic human embryo monitoring by a time-lapse user group. Human Reproduction 29, 2650–2660.
Proposed guidelines on the nomenclature and annotation of dynamic human embryo monitoring by a time-lapse user group.Crossref | GoogleScholarGoogle Scholar |

Desch, L, Bruno, C, Herbemont, C, Michel, F, Bechoua, S, Girod, S, Sagot, P, and Fauque, P (2015). Impact on ICSI outcomes of adding 24 h of in vitro culture before testicular sperm freezing: a retrospective study. Basic and Clinical Andrology 25, 6.
Impact on ICSI outcomes of adding 24 h of in vitro culture before testicular sperm freezing: a retrospective study.Crossref | GoogleScholarGoogle Scholar |

Desch, L, Bruno, C, Luu, M, Barberet, J, Choux, C, Lamotte, M, Schmutz, E, Sagot, P, and Fauque, P (2017). Embryo multinucleation at the two-cell stage is an independent predictor of intracytoplasmic sperm injection outcomes. Fertility and Sterility 107, 97–103.e4.
Embryo multinucleation at the two-cell stage is an independent predictor of intracytoplasmic sperm injection outcomes.Crossref | GoogleScholarGoogle Scholar |

Fauque, P, Audureau, E, Leandri, R, Delaroche, L, Assouline, S, Epelboin, S, Jouannet, P, and Patrat, C (2013). Is the nuclear status of an embryo an independent factor to predict its ability to develop to term? Fertility and Sterility 99, 1299–1304.e3.
Is the nuclear status of an embryo an independent factor to predict its ability to develop to term?Crossref | GoogleScholarGoogle Scholar |

Freour, T, Masson, D, Mirallie, S, Jean, M, Bach, K, Dejoie, T, and Barriere, P (2008). Active smoking compromises IVF outcome and affects ovarian reserve. Reproductive BioMedicine Online 16, 96–102.
Active smoking compromises IVF outcome and affects ovarian reserve.Crossref | GoogleScholarGoogle Scholar |

Fréour, T, Dessolle, L, Lammers, J, Lattes, S, and Barrière, P (2013). Comparison of embryo morphokinetics after in vitro fertilization-intracytoplasmic sperm injection in smoking and nonsmoking women. Fertility and Sterility 99, 1944–1950.
Comparison of embryo morphokinetics after in vitro fertilization-intracytoplasmic sperm injection in smoking and nonsmoking women.Crossref | GoogleScholarGoogle Scholar |

Fuentes, A, Muñoz, A, Barnhart, K, Argüello, B, Díaz, M, and Pommer, R (2010). Recent cigarette smoking and assisted reproductive technologies outcome. Fertility and Sterility 93, 89–95.
Recent cigarette smoking and assisted reproductive technologies outcome.Crossref | GoogleScholarGoogle Scholar |

Gallo, A, Boni, R, and Tosti, E (2020). Gamete quality in a multistressor environment. Environment International 138, 105627.
Gamete quality in a multistressor environment.Crossref | GoogleScholarGoogle Scholar |

Gunes, S, Metin Mahmutoglu, A, Arslan, MA, and Henkel, R (2018). Smoking-induced genetic and epigenetic alterations in infertile men. Andrologia 50, e13124.
Smoking-induced genetic and epigenetic alterations in infertile men.Crossref | GoogleScholarGoogle Scholar |

Huang, J, Okuka, M, McLean, M, Keefe, DL, and Liu, L (2009). Effects of cigarette smoke on fertilization and embryo development in vivo. Fertility and Sterility 92, 1456–1465.
Effects of cigarette smoke on fertilization and embryo development in vivo.Crossref | GoogleScholarGoogle Scholar |

Kapawa, A, Giannakis, D, Tsoukanelis, K, Kanakas, N, Baltogiannis, D, Agapitos, E, Loutradis, D, Miyagawa, I, and Sofikitis, N (2004). Effects of paternal cigarette smoking on testicular function, sperm fertilizing capacity, embryonic development, and blastocyst capacity for implantation in rats. Andrologia 36, 57–68.
Effects of paternal cigarette smoking on testicular function, sperm fertilizing capacity, embryonic development, and blastocyst capacity for implantation in rats.Crossref | GoogleScholarGoogle Scholar |

Kim, H, Kim, SK, Yu, EJ, Lee, JR, Jee, BC, Suh, CS, and Kim, SH (2015). The prevalence of positive urinary cotinine tests in Korean infertile couples and the effect of smoking on assisted conception outcomes. Clinical and Experimental Reproductive Medicine 42, 136–142.
The prevalence of positive urinary cotinine tests in Korean infertile couples and the effect of smoking on assisted conception outcomes.Crossref | GoogleScholarGoogle Scholar |

Künzle, R, Mueller, MD, Hänggi, W, Birkhäuser, MH, Drescher, H, and Bersinger, NA (2003). Semen quality of male smokers and nonsmokers in infertile couples. Fertility and Sterility 79, 287–291.
Semen quality of male smokers and nonsmokers in infertile couples.Crossref | GoogleScholarGoogle Scholar |

Li, Y, Lin, H, Ma, M, Li, L, Cai, M, Zhou, N, Han, X, Bao, H, Huang, L, Zhu, C, Li, C, Yang, H, Rao, Z, Xiang, Y, Cui, Z, Ao, L, Zhou, Z, Xiong, H, and Cao, J (2009). Semen quality of 1346 healthy men, results from the Chongqing area of southwest China. Human Reproduction 24, 459–469.
Semen quality of 1346 healthy men, results from the Chongqing area of southwest China.Crossref | GoogleScholarGoogle Scholar |

Pan, W (2001). Akaike’s information criterion in generalized estimating equations. Biometrics 57, 120–125.
Akaike’s information criterion in generalized estimating equations.Crossref | GoogleScholarGoogle Scholar |

Pappas, RS, Polzin, GM, Zhang, L, Watson, CH, Paschal, DC, and Ashley, DL (2006). Cadmium, lead, and thallium in mainstream tobacco smoke particulate. Food and Chemical Toxicology 44, 714–723.
Cadmium, lead, and thallium in mainstream tobacco smoke particulate.Crossref | GoogleScholarGoogle Scholar |

Parinaud, J, Mieusset, R, Vieitez, G, Labal, B, and Richoilley, G (1993). Influence of sperm parameters on embryo quality. Fertility and Sterility 60, 888–892.
Influence of sperm parameters on embryo quality.Crossref | GoogleScholarGoogle Scholar |

R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at https://www.R-project.org/

Rockhill, K, Tong, VT, Boulet, SL, Zhang, Y, Jamieson, DJ, and Kissin, DM (2019). Smoking and clinical outcomes of assisted reproductive technologies. Journal of Women’s Health 28, 314–322.
Smoking and clinical outcomes of assisted reproductive technologies.Crossref | GoogleScholarGoogle Scholar |

Sapra, KJ, Barr, DB, Maisog, JM, Sundaram, R, and Buck Louis, GM (2016). Time-to-pregnancy associated with couples’ use of tobacco products. Nicotine & Tobacco Research 18, 2154–2161.
Time-to-pregnancy associated with couples’ use of tobacco products.Crossref | GoogleScholarGoogle Scholar |

Sharma, R, Harlev, A, Agarwal, A, and Esteves, SC (2016). 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. European Urology 70, 635–645.
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.Crossref | GoogleScholarGoogle Scholar |

Soares, SR, and Melo, MA (2008). Cigarette smoking and reproductive function. Current Opinion in Obstetrics and Gynecology 20, 281–291.
Cigarette smoking and reproductive function.Crossref | GoogleScholarGoogle Scholar |

Tesarik, J (2005). Paternal effects on cell division in the human preimplantation embryo. Reproductive BioMedicine Online 10, 370–375.
Paternal effects on cell division in the human preimplantation embryo.Crossref | GoogleScholarGoogle Scholar |

Tong, VT, Kissin, DM, Bernson, D, Copeland, G, Boulet, SL, Zhang, Y, Jamieson, DJ, and England, LJ (2016). Maternal smoking among women with and without use of assisted reproductive technologies. Journal of Women’s Health 25, 1066–1072.
Maternal smoking among women with and without use of assisted reproductive technologies.Crossref | GoogleScholarGoogle Scholar |

Trummer, H, Habermann, H, Haas, J, and Pummer, K (2002). The impact of cigarette smoking on human semen parameters and hormones. Human Reproduction 17, 1554–1559.
The impact of cigarette smoking on human semen parameters and hormones.Crossref | GoogleScholarGoogle Scholar |

Vanegas, JC, Chavarro, JE, Williams, PL, Ford, JB, Toth, TL, Hauser, R, and Gaskins, AJ (2017). Discrete survival model analysis of a couple’s smoking pattern and outcomes of assisted reproduction. Fertility Research and Practice 3, 5.
Discrete survival model analysis of a couple’s smoking pattern and outcomes of assisted reproduction.Crossref | GoogleScholarGoogle Scholar |

Waylen, AL, Metwally, M, Jones, GL, Wilkinson, AJ, and Ledger, WL (2009). Effects of cigarette smoking upon clinical outcomes of assisted reproduction: a meta-analysis. Human Reproduction Update 15, 31–44.
Effects of cigarette smoking upon clinical outcomes of assisted reproduction: a meta-analysis.Crossref | GoogleScholarGoogle Scholar |

World Health Organization (2021) ‘WHO global report on trends in prevalence of tobacco smoking 2000–2025.’ 2nd edn. (World Health Organization: Geneva) Available at http://www.who.int/tobacco/publications/surveillance/trends-tobacco-smoking-second-edition/en/. [Accessed 18 May 2021]

Zitzmann, M, Rolf, C, Nordhoff, V, Schräder, G, Rickert-Föhring, M, Gassner, P, Behre, HM, Greb, RR, Kiesel, L, and Nieschlag, E (2003). Male smokers have a decreased success rate for in vitro fertilization and intracytoplasmic sperm injection. Fertility and Sterility 79, 1550–1554.
Male smokers have a decreased success rate for in vitro fertilization and intracytoplasmic sperm injection.Crossref | GoogleScholarGoogle Scholar |