Discrete survival model analysis of a couple's smoking pattern and outcomes of assisted reproduction

Jose C Vanegas, Jorge E Chavarro, Paige L Williams, Jennifer B Ford, Thomas L Toth, Russ Hauser, Audrey J Gaskins, Jose C Vanegas, Jorge E Chavarro, Paige L Williams, Jennifer B Ford, Thomas L Toth, Russ Hauser, Audrey J Gaskins

Abstract

Background: Cigarette smoking has been associated with worse infertility treatment outcomes, yet some studies have found null or inconsistent results.

Methods: We followed 225 couples who underwent 354 fresh non-donor assisted reproductive technology (ART) cycles between 2006 and 2014. Smoking history was self-reported at study entry. We evaluated the associations between smoking patterns and ART success using multivariable discrete time Cox proportional hazards models with six time periods: cycle initiation to egg retrieval, retrieval to fertilization, fertilization to embryo transfer (ET), ET to implantation, implantation to clinical pregnancy, and clinical pregnancy to live birth to estimate hazard ratios (HR) and 95% CIs. Time-dependent interactions between smoking intensity and ART time period were used to identify vulnerable periods.

Results: Overall, 26% of women and 32% of men reported ever smoking. The HR of failing in the ART cycle without attaining live birth for male and female ever smokers was elevated, but non-significant, compared to never smokers regardless of intensity (HR = 1.02 and 1.30, respectively). Female ever smokers were more likely to fail prior to oocyte retrieval (HR: 3.37; 95% CI: 1.00, 12.73). Every one cigarette/day increase in smoking intensity for females was associated with a HR of 1.02 of failing ART (95% CI: 0.97, 1.08), regardless of duration or current smoking status. Women with higher smoking intensities were most likely to fail a cycle prior to oocyte retrieval (HR: 1.07; 95% CI: 1.00, 1.16). Among past smokers, every additional year since a man had quit smoking reduced the risk of failing ART by 4% (HR: 0.96; 95% CI: 0.91, 1.00) particularly between clinical pregnancy and live birth (HR: 0.86; 95% CI: 0.76, 0.96).

Conclusions: Female smoking intensity, regardless of current smoking status, is positively associated with the risk of failing ART cycles between initiation and oocyte retrieval. In men who ever smoked, smoking cessation may reduce the probability of failing ART, particularly between clinical pregnancy and live birth.

Trial registration: NCT00011713. Registered: 27 February 2001.

Keywords: Assisted reproductive technologies; Fertility; Reproductive health; Smoking; Survival analysis; in vitro fertilization.

Conflict of interest statement

Competing interests The authors declare that they have no competing interests.

References

    1. Havelaar AH, Kirk MD, Torgerson PR, Gibb HJ, Hald T, Lake RJ, Praet N, Bellinger DC, de Silva NR, Gargouri N, et al. World Health Organization Global Estimates and Regional Comparisons of the Burden of Foodborne Disease in 2010. PLoS Med. 2015;12:e1001923. doi: 10.1371/journal.pmed.1001923.
    1. World Health Organization (WHO) Tobacco Free Initiative. Geneva: WHO; 2015. WHO report on the global tobacco epidemic, 2015: Raising taxes on tobacco.
    1. Tong VT, Dietz PM, Morrow B, D’Angelo DV, Farr SL, Rockhill KM, England LJ. Trends in smoking before, during, and after pregnancy--Pregnancy Risk Assessment Monitoring System, United States, 40 sites, 2000–2010. MMWR Surveill Summ. 2013;62:1–19.
    1. Agaku IT, King BA, Husten CG, Bunnell R, Ambrose BK, Hu SS, Holder-Hayes E, Day HR. Tobacco product use among adults--United States, 2012–2013. MMWR Morb Mortal Wkly Rep. 2014;63:542–547.
    1. Kaiserman MJ, Rickert WS. Carcinogens in tobacco smoke: benzo[a]pyrene from Canadian cigarettes and cigarette tobacco. Am J Public Health. 1992;82:1023–1026. doi: 10.2105/AJPH.82.7.1023.
    1. Ding YS, Trommel JS, Yan XJ, Ashley D, Watson CH. Determination of 14 polycyclic aromatic hydrocarbons in mainstream smoke from domestic cigarettes. Environ Sci Technol. 2005;39:471–478. doi: 10.1021/es048690k.
    1. Augood C, Duckitt K, Templeton AA. Smoking and female infertility: a systematic review and meta-analysis. Hum Reprod. 1998;13:1532–1539. doi: 10.1093/humrep/13.6.1532.
    1. Jeng HA, Chen YL, Kantaria KN. Association of cigarette smoking with reproductive hormone levels and semen quality in healthy adult men in Taiwan. J Environ Sci Health A Tox Hazard Subst Environ Eng. 2014;49:262–268. doi: 10.1080/10934529.2014.846195.
    1. Waylen AL, Metwally M, Jones GL, Wilkinson AJ, Ledger WL. Effects of cigarette smoking upon clinical outcomes of assisted reproduction: a meta-analysis. Hum Reprod Update. 2009;15:31–44. doi: 10.1093/humupd/dmn046.
    1. Winter E, Wang J, Davies MJ, Norman R. Early pregnancy loss following assisted reproductive technology treatment. Hum Reprod. 2002;17:3220–3223. doi: 10.1093/humrep/17.12.3220.
    1. Penzias AS. Recurrent IVF failure: other factors. Fertil Steril. 2012;97:1033–1038. doi: 10.1016/j.fertnstert.2012.03.017.
    1. Klonoff-Cohen H, Natarajan L, Marrs R, Yee B. Effects of female and male smoking on success rates of IVF and gamete intra-Fallopian transfer. Hum Reprod. 2001;16:1382–1390. doi: 10.1093/humrep/16.7.1382.
    1. Cinar O, Dilbaz S, Terzioglu F, Karahalil B, Yucel C, Turk R, Taskin L, Kose SK. Does cigarette smoking really have detrimental effects on outcomes of IVF? Eur J Obstet Gynecol Reprod Biol. 2014;174:106–110. doi: 10.1016/j.ejogrb.2013.12.026.
    1. Hauser R, Meeker JD, Duty S, Silva MJ, Calafat AM. Altered semen quality in relation to urinary concentrations of phthalate monoester and oxidative metabolites. Epidemiology. 2006;17:682–691. doi: 10.1097/01.ede.0000235996.89953.d7.
    1. Pinsky PF, Zhu CS, Kramer BS. Lung cancer risk by years since quitting in 30+ pack year smokers. J Med Screen. 2015;22:151–157. doi: 10.1177/0969141315579119.
    1. Mok-Lin E, Ehrlich S, Williams PL, Petrozza J, Wright DL, Calafat AM, Ye X, Hauser R. Urinary bisphenol A concentrations and ovarian response among women undergoing IVF. Int J Androl. 2010;33:385–393. doi: 10.1111/j.1365-2605.2009.01014.x.
    1. Maity A, Williams PL, Ryan L, Missmer SA, Coull BA, Hauser R. Analysis of in vitro fertilization data with multiple outcomes using discrete time-to-event analysis. Stat Med. 2014;33:1738–1749. doi: 10.1002/sim.6050.
    1. Missmer SA, Pearson KR, Ryan LM, Meeker JD, Cramer DW, Hauser R. Analysis of multiple-cycle data from couples undergoing in vitro fertilization: methodologic issues and statistical approaches. Epidemiology. 2011;22:497–504. doi: 10.1097/EDE.0b013e31821b5351.
    1. Leffondre K, Abrahamowicz M, Siemiatycki J, Rachet B. Modeling smoking history: a comparison of different approaches. Am J Epidemiol. 2002;156:813–823. doi: 10.1093/aje/kwf122.
    1. Neal MS, Hughes EG, Holloway AC, Foster WG. Sidestream smoking is equally as damaging as mainstream smoking on IVF outcomes. Hum Reprod. 2005;20:2531–2535. doi: 10.1093/humrep/dei080.
    1. Wright KP, Trimarchi JR, Allsworth J, Keefe D. The effect of female tobacco smoking on IVF outcomes. Hum Reprod. 2006;21:2930–2934. doi: 10.1093/humrep/del269.
    1. Fuentes A, Munoz A, Barnhart K, Arguello B, Diaz M, Pommer R. Recent cigarette smoking and assisted reproductive technologies outcome. Fertil Steril. 2010;93:89–95. doi: 10.1016/j.fertnstert.2008.09.073.
    1. Mai Z, Lei M, Yu B, Du H, Liu J. The effects of cigarette smoke extract on ovulation, oocyte morphology and ovarian gene expression in mice. PLoS One. 2014;9:e95945. doi: 10.1371/journal.pone.0095945.
    1. Sadeu JC, Foster WG. Cigarette smoke condensate exposure delays follicular development and function in a stage-dependent manner. Fertil Steril. 2011;95:2410–2417. doi: 10.1016/j.fertnstert.2011.03.072.
    1. Bolumar F, Olsen J, Boldsen J. Smoking reduces fecundity: a European multicenter study on infertility and subfecundity. The European Study Group on Infertility and Subfecundity. Am J Epidemiol. 1996;143:578–587. doi: 10.1093/oxfordjournals.aje.a008788.
    1. Van Voorhis BJ, Syrop CH, Hammitt DG, Dunn MS, Snyder GD. Effects of smoking on ovulation induction for assisted reproductive techniques. Fertil Steril. 1992;58:981–985. doi: 10.1016/S0015-0282(16)55446-6.
    1. Freour T, Masson D, Dessolle L, Allaoua D, Dejoie T, Mirallie S, Jean M, Barriere P. Ovarian reserve and in vitro fertilization cycles outcome according to women smoking status and stimulation regimen. Arch Gynecol Obstet. 2012;285:1177–1182. doi: 10.1007/s00404-011-2172-7.
    1. Weigert M, Hofstetter G, Kaipl D, Gottlich H, Krischker U, Bichler K, Poehl M, Feichtinger W. The effect of smoking on oocyte quality and hormonal parameters of patients undergoing in vitro fertilization-embryo transfer. J Assist Reprod Genet. 1999;16:287–293. doi: 10.1023/A:1020496330424.
    1. Buckley JP, Keil AP, McGrath LJ, Edwards JK. Evolving methods for inference in the presence of healthy worker survivor bias. Epidemiology. 2015;26:204–212. doi: 10.1097/EDE.0000000000000217.
    1. Hyland A, Piazza KM, Hovey KM, Ockene JK, Andrews CA, Rivard C, Wactawski-Wende J. Associations of lifetime active and passive smoking with spontaneous abortion, stillbirth and tubal ectopic pregnancy: a cross-sectional analysis of historical data from the Women’s Health Initiative. Tob Control. 2015;24:328–335. doi: 10.1136/tobaccocontrol-2013-051458.
    1. Caserta D, Bordi G, Di Segni N, D’Ambrosio A, Mallozzi M, Moscarini M. The influence of cigarette smoking on a population of infertile men and women. Arch Gynecol Obstet. 2013;287:813–818. doi: 10.1007/s00404-012-2643-5.
    1. Venners SA, Wang X, Chen C, Wang L, Chen D, Guang W, Huang A, Ryan L, O’Connor J, Lasley B, et al. Paternal smoking and pregnancy loss: a prospective study using a biomarker of pregnancy. Am J Epidemiol. 2004;159:993–1001. doi: 10.1093/aje/kwh128.
    1. Centers for Disease Control and Prevention (CDC) American Society for Reproductive Medicine (ASRM) Society for Assisted Reproductive Technology (SART) Assisted Reproductive Technology National Summary Report. Atlanta: US Dept of Health and Human Services; 2013.
    1. Hauser R, Godfrey-Bailey L, Chen Z. Does the potential for selection bias in semen quality studies depend on study design? Experience from a study conducted within an infertility clinic. Hum Reprod. 2005;20:2579–2583. doi: 10.1093/humrep/dei088.
    1. Soulakova JN, Hartman AM, Liu B, Willis GB, Augustine S. Reliability of adult self-reported smoking history: data from the tobacco use supplement to the current population survey 2002–2003 cohort. Nicotine Tob Res. 2012;14:952–960. doi: 10.1093/ntr/ntr313.

Source: PubMed

Szponzorok és közreműködők

Egészségi állapot

Kábítószer-beavatkozások

3
Iratkozz fel