Hostname: page-component-669899f699-tpknm Total loading time: 0 Render date: 2025-04-27T21:19:22.280Z Has data issue: false hasContentIssue false

Effects of substance exposure on gametes and pre-implantation embryos: a narrative review

Published online by Cambridge University Press:  11 November 2024

Shayesteh Mehdinejadiani
Affiliation:
Department of Reproductive Biology, School of Advanced Medical Sciences and Technologies, Shiraz University of Medical Sciences, Shiraz, Iran
Zahra Khosravizadeh
Affiliation:
Department of Gynecology and Obstetrics, School of Medicine, Arak University of Medical Sciences, Arak, Iran
Akram Alizadeh
Affiliation:
Nervous System Stem Cells Research Center, Semnan University of Medical Sciences, Semnan, Iran Department of Tissue Engineering and Applied Cell Sciences, School of Medicine, Semnan University of Medical Sciences, Semnan, Iran
Nahid Azad*
Affiliation:
Abnormal Uterine Bleeding Research Center, Semnan University of Medical Sciences, Semnan, Iran
*
Corresponding author: Nahid Azad; Email: [email protected]

Abstract

Substance use refers to the consumption of drugs that have varying degrees of impact on a persons’ physical, mental and emotional well-being. While the adverse health effects of drugs have been extensively documented, further research is needed to understand their impact on fertility. Studies have indicated that substance use affects both the male and female reproductive systems. As substance use is more prevalent among young adults compared with the elderly, it appears that individuals of reproductive age are particularly vulnerable to the reproductive impairments associated with substance use. Although numerous studies have reported detrimental effects of substance use on pregnant women and their foetus during the post-implantation stages, there are limited studies on critical pre-implantation period and gamete stages. In this narrative review, we aimed to focus on the most significant evidence regarding the impact of substances on gametes and pre-implantation embryos.

Type
Review Article
Copyright
© The Author(s), 2024. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Abdul-Ghani, R., Qazzaz, M., Dabdoub, N., Muhammad, R. and Abdul-Ghani, A. (2014). Studies on cigarette smoke induced oxidative DNA damage and reduced spermatogenesis in rats.Google Scholar
Agirregoitia, E., Ibarra-Lecue, I., Totorikaguena, L., Mendoza, R., Expósito, A., Matorras, R., Urigüen, L. and Agirregoitia, N. (2015) Dynamics of expression and localization of the cannabinoid system in granulosa cells during oocyte nuclear maturation. Fertility and Sterility, 104(3), 753760.CrossRefGoogle ScholarPubMed
Agirregoitia, E., Peralta, L., Mendoza, R., Expósito, A., Ereño, E. D., Matorras, R. and Agirregoitia, N. (2012) Expression and localization of opioid receptors during the maturation of human oocytes. Reproductive Biomedicine Online 24(5), 550557.CrossRefGoogle ScholarPubMed
Agirregoitia, E., Totorikaguena, L., Expósito, A., Mendoza, R., Matorras, R. and Agirregoitia, N. (2016) Dynamic of expression and localization of cannabinoid-degrading enzymes FAAH and MGLL in relation to CB1 during meiotic maturation of human oocytes. Cell and Tissue Research 365(2), 393401.CrossRefGoogle ScholarPubMed
Ahluwalia, B., Smith, D., Adeyiga, O., Akbasak, B. and Rajguru, S. (1992) Ethanol decreases progesterone synthesis in human placental cells: mechanism of ethanol effect. Alcohol, 9, 395401.CrossRefGoogle Scholar
Ahmadnia, H., Ghanbari, M., Moradi, M. R. and Khajeh, D. M. (2007). Effect of cigarette smoke on spermatogenesis in rats. Urology Journal 4(3), 159163.Google ScholarPubMed
Ajayi, A. F. and Akhigbe, R. E. (2020) Codeine-induced sperm DNA damage is mediated predominantly by oxidative stress rather than apoptosis. Redox Report 25(1), 3340.CrossRefGoogle ScholarPubMed
Akhigbe, R. E., Hamed, M. A., Ajayi, L. O., Anyogu, D. C. and Ajayi, A. F. (2021). In vitro effect of codeine on human sperm motility and DNA integrity.CrossRefGoogle Scholar
Alavi, S. H., Taghavi, M. M. and Moallem, S. A. (2008) Evaluation of effects of methamphetamine repeated dosing on proliferation and apoptosis of rat germ cells. Systems Biology in Reproductive Medicine 54(2), 8591.CrossRefGoogle ScholarPubMed
Albrizio, M., Lacalandra, G. M., Micera, E., Guaricci, A. C., Nicassio, M. and Zarrilli, A. (2010) Delta opioid receptor on equine sperm cells: subcellular localization and involvement in sperm motility analyzed by computer assisted sperm analyzer (CASA). Reproductive Biology and Endocrinology 8(1), 111.CrossRefGoogle ScholarPubMed
Asare-Anane, H., Bannison, S., Ofori, E. K., Ateko, R., Bawah, A., Amanquah, S., Oppong, S., Gandau, B. and Ziem, J. (2016) Tobacco smoking is associated with decreased semen quality. Reproductive Health 13, 16.CrossRefGoogle ScholarPubMed
Azari, O., Emadi, L., Kheirandish, R., Shafiei Bafti, H., Esmaili Nejad, M. R. and Faroghi, F. (2014) The effects of long-term administration of tramadol on epididymal sperm quality and testicular tissue in mice. Iranian Journal of Veterinary Surgery 9(1), 2330.Google Scholar
Banafshi, O., Mohammadi, E., Abdi, M., Ghaderi, E., Assadollahi, V., Erfan, M. B. K., Rezaei, M. J. and Fathi, F. (2022) Effect of cigarette smoke condensate on mouse embryo development and expression of pluripotency and apoptotic genes in vitro. Zygote 30(6), 768772.CrossRefGoogle ScholarPubMed
Barazani, Y., Katz, B. F., Nagler, H. M. and Stember, D. S. (2014) Lifestyle, environment, and male reproductive health. Urologic Clinics 41(1), 5566.Google ScholarPubMed
Bari, M., Battista, N., Pirazzi, V. and Maccarrone, M. (2011) The manifold actions of endocannabinoids on female and male reproductive events. Frontiers in Bioscience 16(498), e516.CrossRefGoogle ScholarPubMed
Bassiony, M. M., Youssef, U. M. and El-Gohari, H. (2020) Free testosterone and prolactin levels and sperm morphology and function among male patients with tramadol abuse: A case-control study. Journal of Clinical Psychopharmacology 40(4), 405408.CrossRefGoogle ScholarPubMed
Beal, M. A., Yauk, C. L. and Marchetti, F. (2017) From sperm to offspring: Assessing the heritable genetic consequences of paternal smoking and potential public health impacts. Mutation Research/Reviews in Mutation Research 773, 2650.CrossRefGoogle ScholarPubMed
Bedi, Y., Chang, R. C., Gibbs, R., Clement, T. M. and Golding, M. C. (2019). Alterations in sperm-inherited noncoding RNAs associate with late-term fetal growth restriction induced by preconception paternal alcohol use. Reproductive Toxicology 87, 1120. https://doi.org/10.1016/j.reprotox.2019.04.006 CrossRefGoogle ScholarPubMed
Blandthorn, J., Leung, L., Loke, Y., Lloyd-Jones, D. M., Thurman, R., Bowman, E. and Bonomo, Y. (2018) Prescription opioid use in pregnancy. The Australian and New Zealand Journal of Obstetrics and Gynaecology 58(5), 494498. https://doi.org/10.1111/ajo.12823 CrossRefGoogle ScholarPubMed
Böttcher, B., Seeber, B., Leyendecker, G. and Wildt, L. (2017) Impact of the opioid system on the reproductive axis. Fertility and Sterility 108(2), 207213. https://doi.org/10.1016/j.fertnstert.2017.06.009 CrossRefGoogle ScholarPubMed
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(1), 3036.Google ScholarPubMed
Brents, L. K. (2016) Focus: sex and gender health: Marijuana, the Endocannabinoid System and the female reproductive system. The Yale Journal of Biology and Medicine 89(2), 175.Google Scholar
Brett, K. M. and Cooper, G. S. (2003). Associations with menopause and menopausal transition in a nationally representative US sample. Maturitas 45(2), 8997.CrossRefGoogle Scholar
Browne, C. J., Godino, A., Salery, M. and Nestler, E. J. (2020) Epigenetic Mechanisms of Opioid Addiction. Biological Psychiatry 87(1), 2233. https://doi.org/10.1016/j.biopsych.2019.06.027 CrossRefGoogle ScholarPubMed
Budani, M. C., Carletti, E. and Tiboni, G. M. (2017) Cigarette smoke is associated with altered expression of antioxidant enzymes in granulosa cells from women undergoing in vitro fertilization. Zygote 25(3), 296303.CrossRefGoogle ScholarPubMed
Buéno, L., Fargeas, M. J., Fioramonti, J. and Menezo, Y. (1986) A tetrapeptide isolated from hamster embryo with central opiate properties on gastrointestinal motility but not pain perception. Life Sciences 39(2), 141146. https://doi.org/10.1016/0024-3205(86)90448-0 CrossRefGoogle Scholar
Butler, C. and Stechlinski, P. (2023) Modeling Opioid Abuse: A Case Study of the Opioid Crisis in New England. Bulletin of Mathematical Biology 85(6), 45. https://doi.org/10.1007/s11538-023-01148-1 CrossRefGoogle ScholarPubMed
Calogero, A. E., Cannarella, R., Agarwal, A., Hamoda, T. A.-A. A.-M., Rambhatla, A., Saleh, R., Boitrelle, F., Ziouziou, I., Toprak, T. and Gul, M. (2023). The renaissance of male infertility management in the golden age of andrology. The World Journal of Men’s Health, 41(2), 237.CrossRefGoogle ScholarPubMed
Carpenter, B. L., Remba, T. K., Thomas, S. L., Madaj, Z., Brink, L., Tiedemann, R. L., Odendaal, H. J. and Jones, P. A. (2021). Oocyte age and preconceptual alcohol use are highly correlated with epigenetic imprinting of a noncoding RNA (nc886). Proceedings of the National Academy of Sciences 118(12), e2026580118.CrossRefGoogle ScholarPubMed
Carroll, K., Pottinger, A. M., Wynter, S. and DaCosta, V. (2020) Marijuana use and its influence on sperm morphology and motility: identified risk for fertility among Jamaican men. Andrology 8(1), 136142. https://doi.org/10.1111/andr.12670 CrossRefGoogle ScholarPubMed
Caserta, D., Bordi, G., Di Segni, N., D’Ambrosio, A., Mallozzi, M. and Moscarini, M. (2013) The influence of cigarette smoking on a population of infertile men and women. Arch Gynecol Obstet 287, 813818. https://doi.org/10.1007/s00404-012-2643-5 CrossRefGoogle ScholarPubMed
Cebral, E., Lasserre, A., Rettori, V. and de Gimeno, M. A. (2000) Alterations in preimplantation in vivo development after preconceptional chronic moderate alcohol consumption in female mice. Alcohol and Alcoholism, 35(4), 336343.CrossRefGoogle ScholarPubMed
Chang, S. H., Kim, C. S., Lee, K. S., Kim, H., Yim, S. V., Lim, Y. J. and Park, S. K. (2007) Premenopausal factors influencing premature ovarian failure and early menopause. Maturitas 58(1), 1930. https://doi.org/10.1016/j.maturitas.2007.04.001 CrossRefGoogle ScholarPubMed
Chen, E. C., Samuels, M. H., Luther, M. F., King, T. S., Eddy, C. A., Siler-Khodr, T. M. and Schenken, R. S. (1998) Cocaine impairs follicular phase pulsatile gonadotropin secretion in rhesus monkeys. The Journal of the Society for Gynecologic Investigation: JSGI 5, 311316.CrossRefGoogle ScholarPubMed
Chen, X., Xu, W., Miao, M., Zhu, Z., Dai, J., Chen, Z., Fang, P., Wu, J., Nie, D. and Wang, L. (2015) Alteration of sperm protein profile induced by cigarette smoking. Acta Biochimica et Biophysica Sinica 47(7), 504515.CrossRefGoogle ScholarPubMed
Chen, Y., Kong, S., Tang, X., Fu, Y., Wang, B., Zhang, S. and Wang, H. (2014) Preimplantation mouse embryo is a target for opioid ligand-receptor signaling. Biology of Reproduction 91(1), 4, 19.CrossRefGoogle ScholarPubMed
Chernov, A., Kovalitskaya, Y. A., Sakharova, N. Y. and Chailakhyan, L. (2009). Influence of [beta]-endorphin on preimplantation development of mouse embryos in vitro. Doklady Biological Sciences,CrossRefGoogle Scholar
Chorbov, V. M., Todorov, A. A., Lynskey, M. T. and Cicero, T. J. (2011) Elevated levels of DNA methylation at the OPRM1 promoter in blood and sperm from male opioid addicts. Journal of Opioid Management 7(4), 258264. https://doi.org/10.5055/jom.2011.0067 CrossRefGoogle ScholarPubMed
Chuffa, L. G. A., Padovani, C. R. and Martinez, F. E. (2009) Ovarian structure and hormonal status of the UChA and UChB adult rats in response to ethanol. Maturitas 62(1), 2129.CrossRefGoogle ScholarPubMed
Ciccarone, D. (2011) Stimulant abuse: pharmacology, cocaine, methamphetamine, treatment, attempts at pharmacotherapy. Primary Care 38(1), 4158. https://doi.org/10.1016/j.pop.2010.11.004 CrossRefGoogle ScholarPubMed
Cooper, G. S., Baird, D. D. and Rebecca Darden, F. (2001) Measures of menopausal status in relation to demographic, reproductive, and behavioral characteristics in a population-based study of women aged 35–49 years. American Journal of Epidemiology 153(12), 11591165.CrossRefGoogle Scholar
Corsi, D. J., Hsu, H., Fell, D. B., Wen, S. W. and Walker, M. (2020) Association of Maternal opioid use in pregnancy with adverse perinatal outcomes in Ontario, Canada, From 2012 to 2018. JAMA Network Open 3(7), e208256. https://doi.org/10.1001/jamanetworkopen.2020.8256 CrossRefGoogle ScholarPubMed
Cupo, A., Menezo, Y. and Bueno, L. (1987) Enkephalin production by the corpus luteum. Neuropeptides 9(3), 237245. https://doi.org/10.1016/0143-4179(87)90044-8 CrossRefGoogle ScholarPubMed
Dai, J.-B., Wang, Z.-X. and Qiao, Z.-D. (2015) The hazardous effects of tobacco smoking on male fertility. Asian Journal of Andrology 17(6), 954960.Google ScholarPubMed
de Angelis, C., Nardone, A., Garifalos, F., Pivonello, C., Sansone, A., Conforti, A., Di Dato, C., Sirico, F., Alviggi, C. and Isidori, A. (2020) Smoke, alcohol and drug addiction and female fertility. Reproductive Biology and Endocrinology 18, 126.CrossRefGoogle ScholarPubMed
Dell’Aquila, M., Casavola, V., Reshkin, S., Albrizio, M., Guerra, L., Maritato, F. and Minoia, P. (2002) Effects of β-endorphin and Naloxone on in vitro maturation of bovine oocytes. Molecular Reproduction and Development: Incorporating Gamete Research 63(2), 210222.CrossRefGoogle ScholarPubMed
DiCarlantonio, G. and Talbot, P. (1999) Inhalation of mainstream and sidestream cigarette smoke retards embryo transport and slows muscle contraction in oviducts of hamsters (Mesocricetus auratus). Biology of Reproduction 61(3), 651656.CrossRefGoogle ScholarPubMed
Dickerson, S. M., Walker, D. M., Reveron, M. E., Duvauchelle, C. L. and Gore, A. C. (2008) The recreational drug ecstasy disrupts the hypothalamic-pituitary-gonadal reproductive axis in adult male rats. Neuroendocrinology 88(2), 95102.CrossRefGoogle ScholarPubMed
Dorjgochoo, T., Kallianpur, A., Gao, Y.-T., Cai, H., Yang, G., Li, H., Zheng, W. and Shu, X. O. (2008) Dietary and lifestyle predictors of age at natural menopause and reproductive span in the Shanghai Women’s Health Study. Menopause 15(5), 924933.CrossRefGoogle ScholarPubMed
Drugs, U. N. O. & Crime. (2018). Drugs and age: Drugs and associated issues among young people and older people. In: United Nations.Google Scholar
Ebrahim, A., Sabry, H., Ali, D., El Fallah, A. and Yossef, D. (2020) Effect of Addiction of Diacetylmorphine on Sperm Ultrastructural Morphology. Benha Journal of Applied Sciences 5(6 part (1)), 5762.CrossRefGoogle Scholar
Faden, A. I. (1984) Endogenous opioids: Physiologic and pathophysiologic actions. The Journal of the American Osteopathic Association 84(9), 129134.CrossRefGoogle ScholarPubMed
Fang, D., Li, C., Yong, L., Feng-Rui, W., Biao, D., Wen-Yong, L. and Rong, W. (2015) Effects of alcohol on H3K9 acetylation in mouse pre-implantation embryos. Zoological Research 36(1), 54.Google Scholar
Faut, M., Rodríguez de Castro, C., Bietto, F. M., Castro, J. A. and Castro, G. D. (2009) Metabolism of ethanol to acetaldehyde and increased susceptibility to oxidative stress could play a role in the ovarian tissue cell injury promoted by alcohol drinking. Toxicology and Industrial Health 25(8), 525538.CrossRefGoogle ScholarPubMed
Favetta, L. (2023) O-053 Link between cannabis use and fertility: effects on gamete competence and early embryonic development. Human Reproduction 38(Supplement_1), dead093. 063.CrossRefGoogle Scholar
Finelli, R., Mottola, F. and Agarwal, A. (2021) Impact of alcohol consumption on male fertility potential: a narrative review. International Journal of Environmental Research and Public Health 19(1), 328. https://doi.org/10.3390/ijerph19010328 CrossRefGoogle ScholarPubMed
Firns, S., Cruzat, V. F., Keane, K. N., Joesbury, K. A., Lee, A. H., Newsholme, P. and Yovich, J. L. (2015) The effect of cigarette smoking, alcohol consumption and fruit and vegetable consumption on IVF outcomes: a review and presentation of original data. Reproductive Biology and Endocrinology 13, 113.CrossRefGoogle ScholarPubMed
Frappier, J., Martinaud, A., Barberet, J., Bruno, C., Guilleman, M., Amblot, C., Guilloteau, A. and Fauque, P. (2022) Effect of paternal smoking on pre-implantation embryonic development: a prospective cohort study. Reproduction, Fertility and Development 34(15), 971979.CrossRefGoogle ScholarPubMed
Freeman, J.R., Whitcomb, B.W., Purdue-Smithe, A.C., Manson, J.E., Langton, C.R., Hankinson, S.E., Rosner, B.A. and Bertone-Johnson, E.R. (2021) Is alcohol consumption associated with risk of early menopause? American Journal of Epidemiology 190(12), 26122617.CrossRefGoogle ScholarPubMed
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(7), 19441950.CrossRefGoogle ScholarPubMed
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. Reprod Biomed 16(1), 96102. https://doi.org/10.1016/s1472-6483(10)60561-5 CrossRefGoogle ScholarPubMed
Fronczak, C. M., Kim, E. D. and Barqawi, A. B. (2012) The insults of illicit drug use on male fertility. Journal of andrology 33(4), 515528.CrossRefGoogle ScholarPubMed
Ganapathy, V. (2011) Drugs of abuse and human placenta. Life Sciences 88(21-22), 926930.CrossRefGoogle ScholarPubMed
Gao, J., Gong, L., Wu, Z., Yang, J., Lin, A. and Bu, W. (2017) Effect of cigarette smoke exposure during pregnancy on offspring of ovarian development and oocyte DNA methylation in female mice. Zhonghua lao Dong wei Sheng zhi ye Bing za zhi= Zhonghua Laodong Weisheng Zhiyebing Zazhi= Chinese Journal of Industrial Hygiene and Occupational Diseases 35(6), 455459.Google ScholarPubMed
Gornalusse, G., Spengler, R. M., Sandford, E., Kim, Y., Levy, C., Tewari, M., Hladik, F. and Vojtech, L. (2023). Men who inject opioids exhibit altered tRNA-Gly-GCC isoforms in semen. Molecular Human Reproduction 29, gaad003.CrossRefGoogle ScholarPubMed
Graham, K., Bernards, S., Knibbe, R., Kairouz, S., Kuntsche, S., Wilsnack, S. C., Greenfield, T. K., Dietze, P., Obot, I. and Gmel, G. (2011) Alcohol-related negative consequences among drinkers around the world. Addiction 106(8), 13911405. https://doi.org/10.1111/j.1360-0443.2011.03425.x CrossRefGoogle ScholarPubMed
Gundersen, T. D., Jørgensen, N., Andersson, A.-M., Bang, A. K., Nordkap, L., Skakkebæk, N. E., Priskorn, L., Juul, A. and Jensen, T. K. (2015) Association between use of marijuana and male reproductive hormones and semen quality: a study among 1,215 healthy young men. American Journal of Epidemiology 182(6), 473481.CrossRefGoogle ScholarPubMed
Haight, S. C., Ko, J. Y., Tong, V. T., Bohm, M. K. and Callaghan, W. M. (2018) Opioid use disorder documented at delivery hospitalization - United States, 1999-2014. Morbidity and Mortality Weekly Report 67(31), 845849. https://doi.org/10.15585/mmwr.mm6731a1 CrossRefGoogle ScholarPubMed
Hamad, M., Shelko, N., Kartarius, S., Montenarh, M. and Hammadeh, M. (2014) Impact of cigarette smoking on histone (H2B) to protamine ratio in human spermatozoa and its relation to sperm parameters. Andrology 2(5), 666677.CrossRefGoogle Scholar
Har-Gil, E., Heled, A., Dixon, M., Ahamed, A. M. S. and Bentov, Y. (2021). The relationship between cannabis use and IVF outcome-a cohort study. J Cannabis Res, 3(1), 42. https://doi.org/10.1186/s42238-021-00099-5 CrossRefGoogle ScholarPubMed
Harlev, A., Agarwal, A., Gunes, S. O., Shetty, A. and du Plessis, S. S. (2015) Smoking and male infertility: an evidence-based review. The World Journal of Men’s Health 33(3), 143.CrossRefGoogle ScholarPubMed
Hassold, T., Abruzzo, M., Adkins, K., Griffin, D., Merrill, M., Millie, E., Saker, D., Shen, J. and Zaragoza, M. (1996) Human aneuploidy: incidence, origin, and etiology. Environmental and olecular Mutagenesis 28(3), 167175.3.0.CO;2-B>CrossRefGoogle ScholarPubMed
Haycock, P. C. and Ramsay, M. (2009) Exposure of mouse embryos to ethanol during preimplantation development: effect on DNA methylation in the h19 imprinting control region. Biology of Reproduction 81(4), 618627.CrossRefGoogle ScholarPubMed
Hill, M., Popov, P., Havlikova, H., Kancheva, L., Vrbikova, J., Meloun, M., Kancheva, R., Cibula, D., Pouzar, V. and Cerny, I. (2005) Reinstatement of serum pregnanolone isomers and progesterone during alcohol detoxification therapy in premenopausal women. Alcoholism: Clinical and Experimental Research 29(6), 10101017.CrossRefGoogle ScholarPubMed
Holbrook, B. D. and Rayburn, W. F. (2014) Teratogenic risks from exposure to illicit drugs. Obstetrics and Gynecology Clinics 41(2), 229239.Google ScholarPubMed
Hugues, J., Coste, T., Perret, G., Jayle, M., Sebaoun, J. and Modigliani, E. (1980) Hypothalamo-pituitary ovarian function in thirty-one women with chronic alcoholism. Clinical Endocrinology 12(6), 543551.CrossRefGoogle ScholarPubMed
Irazusta, J., Valdivia, A., Fernández, D., Agirregoitia, E., Ochoa, C. and Casis, L. (2004) Enkephalin-degrading enzymes in normal and subfertile human semen. Journal of Andrology 25(5), 733739.CrossRefGoogle ScholarPubMed
Jana, K., Samanta, P. K. and De, D. K. (2010) Nicotine diminishes testicular gametogenesis, steroidogenesis, and steroidogenic acute regulatory protein expression in adult albino rats: possible influence on pituitary gonadotropins and alteration of testicular antioxidant status. Toxicological Sciences 116(2), 647659.CrossRefGoogle ScholarPubMed
Jensen, T. K., Gottschau, M., Madsen, J. O. B., Andersson, A.-M., Lassen, T. H., Skakkebæk, N. E., Swan, S. H., Priskorn, L., Juul, A. and Jørgensen, N. (2014) Habitual alcohol consumption associated with reduced semen quality and changes in reproductive hormones; a cross-sectional study among 1221 young Danish men. BMJ Open 4(9), e005462. https://doi.org/10.1136/bmjopen-2014-005462 CrossRefGoogle ScholarPubMed
Kaczmarek, M. (2007) The timing of natural menopause in Poland and associated factors. Maturitas 57(2), 139153.CrossRefGoogle ScholarPubMed
Kalant, H. (2001) The pharmacology and toxicology of “ecstasy”(MDMA) and related drugs. CMAJ : Canadian Medical Association Journal 165(7), 917928.Google ScholarPubMed
Kalyuzhny, A., Hensleigh, H. C., Arvidsson, U. and Elde, R. (1997) Immunocytochemical localization of μ-opioid receptors in follicular cells and preimplantation mouse embryos. Anatomy and Embryology 195, 451455.CrossRefGoogle ScholarPubMed
Kamsani, Y., Rajikin, M., Chatterjee, A., Nor-Ashikin, M. and Nuraliza, A. (2010) Impairment of in vitro embryonic development with a corresponding elevation of oxidative stress following nicotine treatment in mice: Effect of variation in treatment duration. Biomedical Research 21(4), 359364.Google Scholar
Kamsani, Y. S., Rajikin, M. H., Khan, N.-A. M. N., Satar, N. A. and Chatterjee, A. (2013) Nicotine-induced cessation of embryonic development is reversed by γ-tocotrienol in mice. Medical Science Monitor Basic Research 19, 87.CrossRefGoogle ScholarPubMed
Kaufmann, R. A., Savoy-Moore, R. T., Sacco, A. G. and Subramanian, M. G. (1990) The effect of cocaine on oocyte development and the follicular microenvironment in the rabbit. Fertility and Sterility 54(5), 921926.CrossRefGoogle ScholarPubMed
Kim, K.-H., Joo, K.-J., Park, H.-J., Kwon, C.-H., Jang, M.-H. and Kim, C.-J. (2005) Nicotine induces apoptosis in TM3 mouse Leydig cells. Fertility and Sterility 83(4), 10931099.CrossRefGoogle ScholarPubMed
Klonoff-Cohen, H., Lam-Kruglick, P. and Gonzalez, C. (2003) Effects of maternal and paternal alcohol consumption on the success rates of in vitro fertilization and gamete intrafallopian transfer. Fertility and Sterility 79(2), 330339.CrossRefGoogle ScholarPubMed
Klonoff-Cohen, H. S., Natarajan, L. and Chen, R. V. (2006) A prospective study of the effects of female and male marijuana use on in vitro fertilization (IVF) and gamete intrafallopian transfer (GIFT) outcomes. American Journal of Obstetrics and Gynecology 194(2), 369376.CrossRefGoogle ScholarPubMed
Kotova, N., Vare, D., Schultz, N., Gradecka Meesters, D., Stepnik, M., Grawé, J., Helleday, T. and Jenssen, D. (2013) Genotoxicity of alcohol is linked to DNA replication-associated damage and homologous recombination repair. Carcinogenesis 34(2), 325330. https://doi.org/10.1093/carcin/bgs340 CrossRefGoogle ScholarPubMed
Kumar, S. B., Chawla, B., Bisht, S., Yadav, R. K. and Dada, R. (2015) Tobacco use increases oxidative DNA damage in sperm-possible etiology of childhood cancer. Asian Pacific Journal of Cancer Prevention 16(16), 69676972.CrossRefGoogle ScholarPubMed
Kumosani, T., Elshal, M. F., Al-Jonaid, A. and Abduljabar, H. (2008) The influence of smoking on semen quality, seminal microelements and Ca2+-ATPase activity among infertile and fertile men. Clinical Biochemistry 41(14-15), 11991203.CrossRefGoogle ScholarPubMed
Künzle, R., Mueller, M. D., Hänggi, W., Birkhäuser, M. H., Drescher, H. and Bersinger, N. A. (2003). Semen quality of male smokers and nonsmokers in infertile couples. Fertility and Sterility, 79(2), 287291.CrossRefGoogle ScholarPubMed
La Maestra, S., De Flora, S. and Micale, R. T. (2015) Effect of cigarette smoke on DNA damage, oxidative stress, and morphological alterations in mouse testis and spermatozoa. International Journal of Hygiene and Environmental Health 218(1), 117122.CrossRefGoogle ScholarPubMed
Labhart, F., Ferris, J., Winstock, A. and Kuntsche, E. (2017) The country-level effects of drinking, heavy drinking and drink prices on pre-drinking: An international comparison of 25 countries. Drug and Alcohol Review 36(6), 742750. https://doi.org/10.1111/dar.12525 CrossRefGoogle ScholarPubMed
Li, F., Wang, Y., Xu, M., Hu, N., Miao, J., Zhao, Y. and Wang, L. (2022) Single-nucleus RNA Sequencing reveals the mechanism of cigarette smoke exposure on diminished ovarian reserve in mice. Ecotoxicology and Environmental Safety 245, 114093.CrossRefGoogle ScholarPubMed
Linschooten, J. O., Verhofstad, N., Gutzkow, K., Olsen, A.-K., Yauk, C., Oligschläger, Y., Brunborg, G., van Schooten, F. J. and Godschalk, R. W. (2013) Paternal lifestyle as a potential source of germline mutations transmitted to offspring. The FASEB Journal 27(7), 2873.CrossRefGoogle ScholarPubMed
Liu, H., Liu, Z., Lu, T., Zhang, L., Cheng, J., Fu, X. and Hou, Y. (2019) Toxic effects of 1-(N-methyl-N-nitrosamino)-1-(3-pyridinyl)-4-butanal on the maturation and subsequent development of murine oocyte. Ecotoxicology and Environmental Safety 181, 370380.CrossRefGoogle ScholarPubMed
Liu, Y., Li, G. P., Sessions, B. R., Rickords, L. F., White, K. L. and Bunch, T. D. (2008) Nicotine induces multinuclear formation and causes aberrant embryonic development in bovine. Molecular Reproduction and Development: Incorporating Gamete Research 75(5), 801809.CrossRefGoogle ScholarPubMed
López-Cardona, A., Ibarra-Lecue, I., Laguna-Barraza, R., Pérez-Cerezales, S., Urigüen, L., Agirregoitia, N., Gutiérrez-Adán, A. and Agirregoitia, E. (2018) Effect of chronic THC administration in the reproductive organs of male mice, spermatozoa and in vitro fertilization. Biochemical Pharmacology 157, 294303.CrossRefGoogle ScholarPubMed
López-Cardona, A. P., Pérez-Cerezales, S., Fernández-González, R., Laguna-Barraza, R., Pericuesta, E., Agirregoitia, N., Gutiérrez-Adán, A. and Agirregoitia, E. (2017) CB1 cannabinoid receptor drives oocyte maturation and embryo development via PI3K/Akt and MAPK pathways. The FASEB Journal 31(8), 33723382.CrossRefGoogle ScholarPubMed
Lui, S., Jones, R. L., Robinson, N. J., Greenwood, S. L., Aplin, J. D. and Tower, C. L. (2014) Detrimental effects of ethanol and its metabolite acetaldehyde, on first trimester human placental cell turnover and function. Plos One 9(2), e87328.CrossRefGoogle ScholarPubMed
Lwow, F., Mędraś, M., Słowińska-Lisowska, M., Jóźków, P. and Szmigiero, L. (2017) The effect of occasional alcohol drinking on semen quality and sperm morphology among young and healthy Polish men.CrossRefGoogle Scholar
Marchetti, F., Rowan-Carroll, A., Williams, A., Polyzos, A., Berndt-Weis, M. L. and Yauk, C. L. (2011) Sidestream tobacco smoke is a male germ cell mutagen. Proceedings of the National Academy of Sciences 108(31), 1281112814.CrossRefGoogle ScholarPubMed
Marczylo, E. L., Amoako, A. A., Konje, J. C., Gant, T. W. and Marczylo, T. H. (2012). Smoking induces differential miRNA expression in human spermatozoa: a potential transgenerational epigenetic concern? Epigenetics 7(5), 432439.CrossRefGoogle Scholar
McHugh, R. K., Wigderson, S. and Greenfield, S. F. (2014). Epidemiology of substance use in reproductive-age women. Obstetrics and Gynecology Clinics 41(2), 177189.Google ScholarPubMed
McLellan, A. T. (2017). Substance Misuse and Substance use Disorders: Why do they Matter in Healthcare? Transactions of the American Clinical and Climatological Association 128, 112130.Google ScholarPubMed
Misner, M. J., Taborek, A., Dufour, J., Sharifi, L., Khokhar, J. Y. and Favetta, L. A. (2021) Effects of delta-9 tetrahydrocannabinol (THC) on oocyte competence and early embryonic development. Frontiers in Toxicology 3, 14.CrossRefGoogle ScholarPubMed
Mohammadzadeh, E., Amjadi, F.-S., Movahedin, M., Zandieh, Z., Nazmara, Z., Eslahi, N., Shirinbayan, P., Asgari, H. R., Azad, N. and Salimi, M. (2017) In vitro development of embryos from experimentally Kerack-addicted Mice. International Journal of Reproductive BioMedicine 15(7), 413.Google ScholarPubMed
Nardo, L. G., Christodoulou, D., Gould, D., Roberts, S. A., Fitzgerald, C. T. and Laing, I. (2007) Anti-Müllerian hormone levels and antral follicle count in women enrolled in in vitro fertilization cycles: relationship to lifestyle factors, chronological age and reproductive history. Gynecological Endocrinology 23(8), 486493.CrossRefGoogle ScholarPubMed
Nassan, F. L., Arvizu, M., Mínguez-Alarcón, L., Williams, P. L., Attaman, J., Petrozza, J., Hauser, R., Chavarro, J. and G, E. S. T. F. J. B. K. M. (2019 ) Marijuana smoking and markers of testicular function among men from a fertility centre. Human Reproduction, 34(4), 715723.CrossRefGoogle ScholarPubMed
Nazmara, Z., Najafi, M., Movahedin, M., Zandiyeh, Z., Shirinbayan, P., Asgari, H. R., Roshanpajouh, M., Maki, C. B., Bashiri, Z. and Koruji, M. (2020) Correlation Between Protamine-2 and miRNA-122 in Sperm from Heroin-addicted Men: A Case-Control Study. Urology Journal 17(6), 638644. https://doi.org/10.22037/uj.v16i7.5747 Google ScholarPubMed
Nazmara, Z., Najafi, M., Rezaei-Mojaz, S. and Movahedin, M. (2019) The effect of heroin addiction on human sperm parameters, histone-to-protamine transition, and serum sexual hormones levels.Google Scholar
Nazmara, Z., Shirinbayan, P., Reza Asgari, H., Ahadi, R., Asgari, F., Maki, C. B., Fattahi, F., Hosseini, B., Janzamin, E. and Koruji, M. (2021) The epigenetic alterations of human sperm cells caused by heroin use disorder. Andrologia 53(1), e13799. https://doi.org/10.1111/and.13799 CrossRefGoogle ScholarPubMed
Nematollahi Mahani, N., Amini, S., Meibodi, I., Nabipour, F. and Eftekhar Vaghefi, H. (2005) Effects of morphine dependency on the ovarian folliculogenesis following superovulation in mice. Journal of Kerman University of Medical Sciences 12(3), 174180.Google Scholar
Nezhad, S. M., GHAFFARI, N. M., FADAEE, F. F., Salehi, M., Salimi, M., SHAMS, M. Z. and Hadi, M. (2016). The effect of methamphetamine on oocyte quality, fertilization rate and embryo development in mice.Google Scholar
Nicolau, P., Miralpeix, E., Sola, I., Carreras, R. and Checa, M. A. (2014) Alcohol consumption and in vitro fertilization: a review of the literature. Gynecological Endocrinology 30(11), 759763.CrossRefGoogle ScholarPubMed
Olabarrieta, E., Totorikaguena, L., Agirregoitia, N. and Agirregoitia, E. (2019) Implication of mu opioid receptor in the in vitro maturation of oocytes and its effects on subsequent fertilization and embryo development in mice. Molecular Reproduction and Development 86(9), 12361244.CrossRefGoogle ScholarPubMed
Omolaoye, T. S., El Shahawy, O., Skosana, B. T., Boillat, T., Loney, T. and Du Plessis, S. S. (2022) The mutagenic effect of tobacco smoke on male fertility. Environmental Science and Pollution Research 29(41), 6205562066.CrossRefGoogle ScholarPubMed
Ozbakir, B. and Tulay, P. (2021) Should fertile women quit drinking alcohol to produce better quality oocytes? Zygote 29(2), 176178.CrossRefGoogle ScholarPubMed
Panlilio, L. V., Goldberg, S. R. and Justinova, Z. (2015) Cannabinoid abuse and addiction: Clinical and preclinical findings. Clinical Pharmacology & Therapeutics 97(6), 616627. https://doi.org/10.1002/cpt.118 CrossRefGoogle ScholarPubMed
Paria, B., Ma, W., Andrenyak, D., Schmid, P., Schmid, H., Moody, D., Deng, H., Makriyannis, A. and Dey, S. (1998) Effects of cannabinoids on preimplantation mouse embryo development and implantation are mediated by brain-type cannabinoid receptors. Biology of Reproduction 58(6), 14901495.CrossRefGoogle ScholarPubMed
Parolini, M., Bini, L., Magni, S., Rizzo, A., Ghilardi, A., Landi, C., Armini, A., Del Giacco, L. and Binelli, A. (2018) Exposure to cocaine and its main metabolites altered the protein profile of zebrafish embryos. Environmental Pollution 232, 603614.CrossRefGoogle ScholarPubMed
Pereira, C. S., Juchniuk de Vozzi, M. S., Dos Santos, S. A., Vasconcelos, M. A. C., de Paz, C. C., Squire, J. A. and Martelli, L. (2014) Smoking-induced chromosomal segregation anomalies identified by FISH analysis of sperm. Molecular Cytogenetics 7, 18.CrossRefGoogle ScholarPubMed
Petrushevska, T. and Velik Stefanovska, V. (2015) Use of Medicines from the Group of Benzodiazepines in the Period of 2003-2013 Year in the Republic of Macedonia. Open Access Macedonian Journal of Medical Sciences 3(1), 151157. https://doi.org/10.3889/oamjms.2015.004 CrossRefGoogle Scholar
Phillips, J. K., Ford, M. A. and Bonnie, R. J. (2017). Pain management and the opioid epidemic: Balancing societal and individual benefits and risks of prescription opioid use.Google Scholar
Potter, D. A., Luther, M. F., Eddy, C. A., Siler-Khodr, T. M., King, T. S. and Schenken, R. S. (1999) Low-dose follicular-phase cocaine administration disrupts menstrual and ovarian cyclicity in rhesus monkeys. The Journal of the Society for Gynecologic Investigation: JSGI 6, 8894.CrossRefGoogle ScholarPubMed
Prasad, M. and Jones, M. (2019) Medical complications of opioid use disorder in pregnancy. Seminars in Perinatology 43(3), 162167. https://doi.org/10.1053/j.semperi.2019.01.005 CrossRefGoogle ScholarPubMed
Price, L. R. and Martinez, J. (2019) Cardiovascular, carcinogenic and reproductive effects of nicotine exposure: A narrative review of the scientific literature. F1000Research 8, 1586. https://doi.org/10.12688/f1000research.20062.2 CrossRefGoogle ScholarPubMed
Racowsky, C., Hendricks, R. C. and Baldwin, K. V. (1989) Direct effects of nicotine on the meiotic maturation of hamster oocytes. Reproductive Toxicology 3(1), 1321.CrossRefGoogle ScholarPubMed
Ragni, G., de Lauretis, L., Bestetti, O., Sghedoni, D. and Aro, V. G. A. (1988) Gonadal function in male heroin and methadone addicts. International Journal of Andrology 11(2), 93100.CrossRefGoogle ScholarPubMed
Rezaei-Mojaz, S., Nazmara, Z., Najafi, M., Movahedin, M., Zandieh, Z., Shirinbayan, P., Roshanpajouh, M., Asgari, H. R., Abbasi, M. and Koruji, M. (2020) Evaluation of enkephalin-degrading enzymes in sperm from heroin-addicted men. International Journal of Fertility & Sterility 13(4), 301.Google ScholarPubMed
Rompala, G. R., Mounier, A., Wolfe, C. M., Lin, Q., Lefterov, I. and Homanics, G. E. (2018) Heavy Chronic Intermittent Ethanol Exposure Alters Small Noncoding RNAs in Mouse Sperm and Epididymosomes. Frontiers in Genetics 9, 32. https://doi.org/10.3389/fgene.2018.00032 CrossRefGoogle ScholarPubMed
Rossi, B. V., Berry, K. F., Hornstein, M. D., Cramer, D. W., Ehrlich, S. and Missmer, S. A. (2011) Effect of alcohol consumption on in vitro fertilization. Obstetrics & Gynecology 117(1), 136142.CrossRefGoogle ScholarPubMed
Roussin, A., Soeiro, T., Fouque, C., Jouanjus, E., Frauger, E., Fouilhé, N., Mallaret, M., Micallef, J. and Lapeyre-Mestre, M. (2022) Increase of high-risk tramadol use and harmful consequences in France from 2013 to 2018: Evidence from the triangulation of addictovigilance data. British Journal of Clinical Pharmacology 88(8), 37893802. https://doi.org/10.1111/bcp.15323 CrossRefGoogle ScholarPubMed
Saberi, A., Sepehri, G., Safi, Z., Razavi, B., Jahandari, F., Divsalar, K. and Salarkia, E. (2017) Effects of methamphetamine on testes histopathology and spermatogenesis indices of adult male rats. Addiction & Health 9(4), 199.Google ScholarPubMed
Safarinejad, M. R., Asgari, S. A., Farshi, A., Ghaedi, G., Kolahi, A. A., Iravani, S. and Khoshdel, A. R. (2013) The effects of opiate consumption on serum reproductive hormone levels, sperm parameters, seminal plasma antioxidant capacity and sperm DNA integrity. Reproductive Toxicology 36, 1823.CrossRefGoogle ScholarPubMed
Sandor, S., Garban, Z., Checiu, M. and Daradics, L. (1981) The presence of ethanol in the oviductal and uterine luminal fluids of alcoholized rats. Morphologie et Embryologie 27(4), 303309.Google ScholarPubMed
Sansone, A., Di Dato, C., de Angelis, C., Menafra, D., Pozza, C., Pivonello, R., Isidori, A. and Gianfrilli, D. (2018) Smoke, alcohol and drug addiction and male fertility. Reproductive Biology and Endocrinology 16, 111.CrossRefGoogle ScholarPubMed
Shah, D. S., Turner, E. L., Chroust, A. J., Duvall, K. L., Wood, D. L. and Bailey, B. A. (2022) Marijuana use in opioid exposed pregnancy increases risk of preterm birth. The Journal of Maternal-Fetal & Neonatal Medicine 35(25), 84568461. https://doi.org/10.1080/14767058.2021.1980532 CrossRefGoogle ScholarPubMed
Shiloh, H., Baratz, S. L., Koifman, M., Ishai, D., Bidder, D., Weiner-Meganzi, Z. and Dirnfeld, M. (2004) The impact of cigarette smoking on zona pellucida thickness of oocytes and embryos prior to transfer into the uterine cavity. Human Reproduction 19(1), 157159.CrossRefGoogle ScholarPubMed
Shrivastava, V., Marmor, H., Chernyak, S., Goldstein, M., Feliciano, M. and Vigodner, M. (2014) Cigarette smoke affects posttranslational modifications and inhibits capacitation-induced changes in human sperm proteins. Reproductive Toxicology 43, 125129.CrossRefGoogle ScholarPubMed
Sinkó, I., Mórocz, M., Zádori, J., Kokavszky, K. and Raskó, I. (2005) Effect of cigarette smoking on DNA damage of human cumulus cells analyzed by comet assay. Reproductive Toxicology 20(1), 6571.CrossRefGoogle ScholarPubMed
Sobinoff, A. P., Beckett, E. L., Jarnicki, A. G., Sutherland, J. M., McCluskey, A., Hansbro, P. M. and McLaughlin, E. A. (2013) Scrambled and fried: cigarette smoke exposure causes antral follicle destruction and oocyte dysfunction through oxidative stress. Toxicology and Applied Pharmacology 271(2), 156167.CrossRefGoogle ScholarPubMed
Srinivasan, M., Hamouda, R. K., Ambedkar, B., Arzoun, H. I., Sahib, I., Fondeur, J., Mendez, L. E., Mohammed, L. and Arzoun, H. (2021) The effect of marijuana on the incidence and evolution of male infertility: a Ssystematic review. Cureus 13(12), e20119.Google ScholarPubMed
Sun, X. and Dey, S. K. (2008) Aspects of endocannabinoid signaling in periimplantation biology. Molecular and Cellular Endocrinology 286(1-2), S3S11.CrossRefGoogle ScholarPubMed
Taniguchi, R., Hatakeyama, S., Ohgi, S. and Yanaihara, A. (2024) Effect of male cigarette smoking on in vitro fertilization (IVF) outcomes and embryo morphokinetic parameters. Cureus 16(1), e52788.Google ScholarPubMed
Viloria, T., Meseguer, M., Martínez-Conejero, J. A., O’Connor, J., Remohí, J., Pellicer, A. and Garrido, N. (2010) Cigarette smoking affects specific sperm oxidative defenses but does not cause oxidative DNA damage in infertile men. Fertility and Sterility 94(2), 631637.CrossRefGoogle Scholar
Walker, O.S., Holloway, A.C. and Raha, S. (2019) The role of the endocannabinoid system in female reproductive tissues. Journal of Ovarian Research 12, 3.CrossRefGoogle ScholarPubMed
Wallén, E., Auvinen, P. and Kaminen-Ahola, N. (2021) The effects of early prenatal alcohol exposure on epigenome and embryonic development. Genes 12(7), 1095.CrossRefGoogle ScholarPubMed
Wang, L., Qu, G., Dong, X., Huang, K., Kumar, M., Ji, L., Wang, Y., Yao, J., Yang, S. and Wu, R. (2016) Long-term effects of methamphetamine exposure in adolescent mice on the future ovarian reserve in adulthood. Toxicology Letters 242, 18.CrossRefGoogle ScholarPubMed
Wiebold, J. and Becker, W. (1987) In-vivo and in-vitro effects of ethanol on mouse preimplantation embryos. Reproduction 80(1), 4957.CrossRefGoogle ScholarPubMed
Wilhoit, L. F., Scott, D. A. and Simecka, B. A. (2017) Fetal alcohol spectrum disorders: characteristics, complications, and treatment. Community Mental Health Journal 53, 711718.CrossRefGoogle Scholar
Wimalasena, J., Meehan, D., Dostal, R. and de Silva, M. (1993) Selective inhibition of luteinizing hormone action by ethanol in cultured human granulosa cells. Alcohol, Clinical and Experimental Research 17, 340344.CrossRefGoogle ScholarPubMed
Wright, C., Milne, S. and Leeson, H. (2014) Sperm DNA damage caused by oxidative stress: modifiable clinical, lifestyle and nutritional factors in male infertility. Reproductive Biomedicine Online 28(6), 684703.CrossRefGoogle ScholarPubMed
Wu, L. T., Ringwalt, C. L., Mannelli, P. and Patkar, A. A. (2008) Hallucinogen use disorders among adult users of MDMA and other hallucinogens. American Journal on Addictions 17(5), 354363. https://doi.org/10.1080/10550490802269064 CrossRefGoogle ScholarPubMed
Yamamoto, Y., Yamamoto, K., Abiru, H., Fukui, Y. and Shiota, K. (1995) Effects of methamphetamine on rat embryos cultured in vitro. Neonatology 68(1), 3338.CrossRefGoogle ScholarPubMed
Yamamoto, Y., Yamamoto, K., Hayase, T., Abiru, H., Shiota, K. and Mori, C. (2002) Methamphetamine induces apoptosis in seminiferous tubules in male mice testis. Toxicology and Applied Pharmacology 178(3), 155160.CrossRefGoogle ScholarPubMed
Yeung, C.-H., Tuettelmann, F., Bergmann, M., Nordhoff, V., Vorona, E. and Cooper, T. G. (2009) Coiled sperm from infertile patients: characteristics, associated factors and biological implication. Human Reproduction 24(6), 12881295.CrossRefGoogle ScholarPubMed
Yingst, J. M., Foulds, J., Veldheer, S., Hrabovsky, S., Trushin, N., Eissenberg, T. T., Williams, J., Richie, J. P., Nichols, T. T., Wilson, S. J. and Hobkirk, A. L. (2019) Nicotine absorption during electronic cigarette use among regular users. PLoS One 14(7), e0220300. https://doi.org/10.1371/journal.pone.0220300 CrossRefGoogle ScholarPubMed
Zalata, A. A., Ahmed, A. H., Allamaneni, S., Comhaire, F. H. and Agarwal, A. (2004) Relationship between acrosin activity of human spermatozoa and oxidative stress. Asian Journal of Andrology 6(4), 313318.Google ScholarPubMed
Zavos, P. M., Correa, J. R., Karagounis, C. S., Ahparaki, A., Phoroglou, C., Hicks, C. L. and Zarmakoupis-Zavos, P. N. (1998) An electron microscope study of the axonemal ultrastructure in human spermatozoa from male smokers and nonsmokers. Fertility and Sterility 69(3), 430434.CrossRefGoogle Scholar
Zhao, S., Chen, F., Feng, A., Han, W. and Zhang, Y. (2019) Risk factors and prevention strategies for postoperative opioid abuse. Pain Research & Management 2019, 7490801. https://doi.org/10.1155/2019/7490801 CrossRefGoogle ScholarPubMed