Hostname: page-component-6b989bf9dc-94dtm Total loading time: 0 Render date: 2024-04-13T11:11:41.092Z Has data issue: false hasContentIssue false

Effects of cigarette smoke condensate on reproduction in mice in vivo

Published online by Cambridge University Press:  11 April 2023

Omid Banafshi
Affiliation:
Cellular and Molecular Research Center, Research Institute for Health Development, Kurdistan University of Medical Sciences, Sanandaj, Iran Zoonoses Research Center, Research Institute for Health Development, Kurdistan University of Medical Sciences, Sanandaj, Iran
Mohammad Abdi
Affiliation:
Cellular and Molecular Research Center, Research Institute for Health Development, Kurdistan University of Medical Sciences, Sanandaj, Iran
Vahideh Assadollahi
Affiliation:
Cellular and Molecular Research Center, Research Institute for Health Development, Kurdistan University of Medical Sciences, Sanandaj, Iran
Ebrahim Mohammadi
Affiliation:
Environmental Health Research Center, Research Institute for Health Development, Kurdistan University of Medical Sciences, Sanandaj, Iran Department of Occupational Health Engineering, Faculty of Health, Kurdistan University of Medical Sciences, Sanandaj, Iran
Ebrahim Ghaderi
Affiliation:
Zoonoses Research Center, Research Institute for Health Development, Kurdistan University of Medical Sciences, Sanandaj, Iran
Mohammad Bagher Khadem Erfan
Affiliation:
Cellular and Molecular Research Center, Research Institute for Health Development, Kurdistan University of Medical Sciences, Sanandaj, Iran
Mohammad Jafar Rezaei
Affiliation:
Cellular and Molecular Research Center, Research Institute for Health Development, Kurdistan University of Medical Sciences, Sanandaj, Iran
Vida Aghamiri
Affiliation:
Department of Midwifery, Faculty of Nursing and Midwifery, Kurdistan University of Medical Sciences, Sanandaj, Iran
Fardin Fathi*
Affiliation:
Cellular and Molecular Research Center, Research Institute for Health Development, Kurdistan University of Medical Sciences, Sanandaj, Iran
*
Author for correspondence: Fardin Fathi. Kurdistan University of Medical Sciences, Pasdaran St, Sanandaj 6617755445, Iran. Tel: +98 9183735091. E-mail: farfath@gmail.com

Summary

Smoking has dangerous and sometimes irreversible effects on various body tissues, including the reproductive system. We conducted this research to determine the in vivo effects of cigarette smoke condensate (CSC) on reproduction in mice. In this experimental in vivo study, 32 male and female NMRI mice were divided into four groups. The mice were injected with CSC (CSC-1R3F) for 28 days. The mice were mated 1 day after the last injection and observed daily for 1 week for the presence of a vaginal plug to track mating. We evaluated mating success rate, and sperm and oocyte quality, pregnancy outcome, childbearing status, and in vitro fertilization (IVF). The results showed a decrease in successful mating in female mice that received the CSC injections. CSC significantly influenced the number of offspring born to males. When the CSC was injected into male mice, there was a significant increase in the number of offspring compared with the group in which only the females received CSC injections. According to the results, there was a negative effect of CSC on morphological parameters in male and female mice. Also, successful IVF after exposure to CSC was significantly decreased in the female mice treated group. The results indicated that CSC significantly affected the number of offspring and fecundity success in females.

Type
Research Article
Copyright
© The Author(s), 2023. 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.)

References

Al-Mukhaini, N., Ba Omar, T. B., Eltayeb, E., Al-Shehi, A. A. K., Al-Belushi, J., Al-Riyami, N., Cipriano, R. and Al-Adawi, K. (2020) Effect of smokeless tobacco product, Afzal, on the reproductive hormones and gonadal pathology of Wistar rats. Sultan Qaboos University Journal for Science [SQUJS], 25(1), 19. doi: 10.24200/squjs.vol25iss1pp1-9 CrossRefGoogle Scholar
Assadollahi, V., Mohammadi, E., Fathi, F., Hassanzadeh, K., Erfan, M. B. K., Soleimani, F., Banafshi, O., Yosefi, F. and Allahvaisi, O. (2019) Effects of cigarette smoke condensate on proliferation and pluripotency gene expression in mouse embryonic stem cells. Journal of Cellular Biochemistry, 120(3), 40714080. doi: 10.1002/jcb.27692 CrossRefGoogle ScholarPubMed
Audi, S. S., Abraham, M. E. and Borker, A. S. (2006). Effect of cigarette smoke on body weight, food intake and reproductive organs in adult albino rats. Indian Journal of Experimental Biology, 44(7), 562565.Google ScholarPubMed
Aydos, K., Güven, M. C., Can, B. and Ergün, A. (2001). Nicotine toxicity to the ultrastructure of the testis in rats. BJU International, 88(6), 622626. doi: 10.1046/j.1464-4096.2001.02384.x CrossRefGoogle Scholar
Azad, F., Nejati, V., Shalizar-Jalali, A., Najafi, G. and Rahmani, F. (2018). Royal jelly protects male mice against nicotine-induced reproductive failure. Veterinary Research Forum, 9(3), 231238. doi: 10.30466/vrf.2018.32088 Google ScholarPubMed
Budin, S. B., Kho, J. H., Lee, J. H., Ramalingam, A., Jubaidi, F. F., Latif, E. S., Zainalabidin, S., Taib, I. S. and Mohamed, J. (2017). Low-dose nicotine exposure induced the oxidative damage of reproductive organs and altered the sperm characteristics of adolescent male rats. Malaysian Journal of Medical Sciences: MJMS, 24(6), 5057. doi: 10.21315/mjms2017.24.6.6 CrossRefGoogle ScholarPubMed
Carmines, E. L., Gaworski, C. L., Faqi, A. S. and Rajendran, N. (2003). In utero exposure to 1R4F reference cigarette smoke: Evaluation of developmental toxicity. Toxicological Sciences, 75(1), 134147. doi: 10.1093/toxsci/kfg155 CrossRefGoogle ScholarPubMed
Chohan, K. R. and Badawy, S. Z. A. (2010). Cigarette smoking impairs sperm bioenergetics. International Brazilian Journal of Urology, 36(1), 6065. doi: 10.1590/s1677-55382010000100010 CrossRefGoogle ScholarPubMed
Csiszar, A., Labinskyy, N., Podlutsky, A., Kaminski, P. M., Wolin, M. S., Zhang, C., Mukhopadhyay, P., Pacher, P., Hu, F., de Cabo, R., Ballabh, P. and Ungvari, Z. (2008). Vasoprotective effects of resveratrol and SIRT1: Attenuation of cigarette smoke-induced oxidative stress and proinflammatory phenotypic alterations. American Journal of Physiology. Heart and Circulatory Physiology, 294(6), H2721H2735. doi: 10.1152/ajpheart.00235.2008 CrossRefGoogle ScholarPubMed
Darbandi, M., Darbandi, S., Agarwal, A., SenGupta, P., Durairajanayagam, D., Henkel, R. and Sadeghi, M. R. (2018). Reactive oxygen species and male reproductive hormones. Reproductive Biology and Endocrinology: RB&E, 16(1), 87. doi: 10.1186/s12958-018-0406-2 CrossRefGoogle ScholarPubMed
de Angelis, C., Nardone, A., Garifalos, F., Pivonello, C., Sansone, A., Conforti, A., Di Dato, C., Sirico, F., Alviggi, C., Isidori, A., Colao, A. and Pivonello, R. (2020). Smoke, alcohol and drug addiction and female fertility. Reproductive Biology and Endocrinology: RB&E, 18(1), 21. doi: 10.1186/s12958-020-0567-7 CrossRefGoogle ScholarPubMed
de Souza, M. daS., Lima, P. H., Sinzato, Y. K., Rudge, M. V., Pereira, O. C. and Damasceno, D. C. (2009). Effects of cigarette smoke exposure on pregnancy outcome and offspring of diabetic rats. Reproductive Biomedicine Online, 18(4), 562567. doi: 10.1016/s1472-6483(10)60135-6 CrossRefGoogle ScholarPubMed
Farber, H. J., Groner, J., Walley, S., Nelson, K. and SECTION ON TOBACCO CONTROL. (2015). Protecting children from tobacco, nicotine, and tobacco smoke. Pediatrics, 136(5), e1439e1467. doi: 10.1542/peds.2015-3110 CrossRefGoogle ScholarPubMed
Florek, E., Janicki, R., Piekoszewski, W., Kulza, M., Chuchracki, M. and Sedziak, A. (2008). Tobacco smoking influence on the level of sex hormones—Animal model. Przegląd Lekarski, 65(10), 508513.Google ScholarPubMed
Florescu, A., Ferrence, R., Einarson, T., Selby, P., Soldin, O. and Koren, G. (2009). Methods for quantification of exposure to cigarette smoking and environmental tobacco smoke: Focus on developmental toxicology. Therapeutic Drug Monitoring, 31(1), 1430. doi: 10.1097/FTD.0b013e3181957a3b CrossRefGoogle ScholarPubMed
Gavriliouk, D. and Aitken, R. J. (2015). Damage to sperm DNA mediated by reactive oxygen species: its impact on human reproduction and the health trajectory of offspring. Advances in Experimental Medicine and Biology, 868, 2347. doi: 10.1007/978-3-319-18881-2_2 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. World Journal of Men’s Health, 33(3), 143160. doi: 10.5534/wjmh.2015.33.3.143 CrossRefGoogle ScholarPubMed
Huang, J., Okuka, M., McLean, M., Keefe, D. L. and Liu, L. (2009). Effects of cigarette smoke on fertilization and embryo development in vivo . Fertility and Sterility, 92(4), 14561465. doi: 10.1016/j.fertnstert.2008.07.1781 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) (Suppl. 1), 1093–1099. doi: 10.1016/j.fertnstert.2004.12.013 CrossRefGoogle ScholarPubMed
Isiegas, C., Mague, S. D. and Blendy, J. A. (2009). Sex differences in response to nicotine in C57BL/6: 129SvEv mice. Nicotine and Tobacco Research, 11(7), 851858. doi: 10.1093/ntr/ntp076 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. doi: 10.1093/toxsci/kfq149 CrossRefGoogle ScholarPubMed
Kaplan, A., Abidi, E., Ghali, R., Booz, G. W., Kobeissy, F. and Zouein, F. A. (2017). Functional, cellular, and molecular remodeling of the heart under influence of oxidative cigarette tobacco smoke. Oxidative Medicine and Cellular Longevity, 2017, 3759186. doi: 10.1155/2017/3759186 CrossRefGoogle ScholarPubMed
Kapoor, D. and Jones, T. H. (2005). Smoking and hormones in health and endocrine disorders. European Journal of Endocrinology, 152(4), 491499. doi: 10.1530/eje.1.01867 CrossRefGoogle ScholarPubMed
Lim, J. and Luderer, U. (2011). Oxidative damage increases and antioxidant gene expression decreases with aging in the mouse ovary. Biology of Reproduction, 84(4), 775782. doi: 10.1095/biolreprod.110.088583 CrossRefGoogle ScholarPubMed
Mai, Z., Lei, M., Yu, B., Du, H. and Liu, J. (2014). The effects of cigarette smoke extract on ovulation, oocyte morphology and ovarian gene expression in mice. PLOS ONE, 9(4), e95945. doi: 10.1371/journal.pone.0095945 CrossRefGoogle ScholarPubMed
Mendelson, J. H., Sholar, M. B., Mutschler, N. H., Jaszyna-Gasior, M., Goletiani, N. V., Siegel, A. J. and Mello, N. K. (2003). Effects of intravenous cocaine and cigarette smoking on luteinizing hormone, testosterone, and prolactin in men. Journal of Pharmacology and Experimental Therapeutics, 307(1), 339348. doi: 10.1124/jpet.103.052928 CrossRefGoogle ScholarPubMed
Mostafa, R. M., Nasrallah, Y. S., Hassan, M. M., Farrag, A. F., Majzoub, A. and Agarwal, A. (2018). The effect of cigarette smoking on human seminal parameters, sperm chromatin structure and condensation. Andrologia, 50(3), e12910. doi: 10.1111/and.12910 CrossRefGoogle ScholarPubMed
Nadeem, F., Fahim, A. and Bugti, S. (2012). Effects of cigarette smoking on male fertility. Turkish Journal of Medical Sciences, 42(Suppl. 2), 14001405. doi: 10.3906/sag-1107-25 Google Scholar
Nesseim, W. H., Haroun, H. S., Mostafa, E., Youakim, M. F. and Mostafa, T. (2011). Effect of nicotine on spermatogenesis in adult albino rats. Andrologia, 43(6), 398404. doi: 10.1111/j.1439-0272.2010.01086.x CrossRefGoogle ScholarPubMed
Olooto, W. E., Amballi, A. A. and Banjo, Taiwo A. (2012). A review of female infertility; important etiological factors and management. Journal of Microbiology and Biotechnology Research, 2(3), 379385.Google Scholar
Onor, I. O., Stirling, D. L., Williams, S. R., Bediako, D., Borghol, A., Harris, M. B., Darensburg, T. B., Clay, S. D., Okpechi, S. C. and Sarpong, D. F. (2017). Clinical effects of cigarette smoking: Epidemiologic impact and review of pharmacotherapy options. International Journal of Environmental Research and Public Health, 14(10), 1147. doi: 10.3390/ijerph14101147 CrossRefGoogle ScholarPubMed
Oyeyipo, I. P., Raji, Y., Emikpe, B. O. and Bolarinwa, A. F. (2011). Effects of nicotine on sperm characteristics and fertility profile in adult male rats: A possible role of cessation. Journal of Reproduction and Infertility, 12(3), 201207.Google ScholarPubMed
Ozgur, K., Isikoglu, M., Seleker, M. and Donmez, L. (2005). Semen quality of smoking and non-smoking men in infertile couples in a Turkish population. Archives of Gynecology and Obstetrics, 271(2), 109112. doi: 10.1007/s00404-003-0572-z CrossRefGoogle Scholar
Rogers, J. M. (2009). Tobacco and pregnancy. Reproductive Toxicology, 28(2), 152160. doi: 10.1016/j.reprotox.2009.03.012 CrossRefGoogle ScholarPubMed
Szkup, M., Jurczak, A., Karakiewicz, B., Kotwas, A., Kopeć, J. and Grochans, E. (2018). Influence of cigarette smoking on hormone and lipid metabolism in women in late reproductive stage. Clinical Interventions in Aging, 13, 109115. doi: 10.2147/CIA.S140487 CrossRefGoogle ScholarPubMed
Wilks, D. J. and Hay, A. W. M. (2004). Smoking and female fecundity: The effect and importance of study design. European Journal of Obstetrics, Gynecology, and Reproductive Biology, 112(2), 127135. doi: 10.1016/s0301-2115(03)00332-4 CrossRefGoogle ScholarPubMed
Woodward, B. and Mehta, J. (Eds). (2019). Female infertility: Core principles and clinical management. JP Medical Ltd.Google Scholar
Zhang, J. P., Meng, Q. Y., Wang, Q., Zhang, L. J., Mao, Y. L. and Sun, Z. X. (2000). Effect of smoking on semen quality of infertile men in Shandong, China. Asian Journal of Andrology, 2(2), 143146.Google ScholarPubMed