Skip to main content

Advertisement

SpringerLink
Log in

Maternal Oxidative Stress, Placental Morphometry, and Fetal Growth in Diabetic Rats Exposed to Cigarette Smoke

  • Original Article
  • Published:
Reproductive Sciences Aims and scope Submit manuscript

Abstract

The diabetic syndrome affects pregnancy, contributing to placental functional and structural disruptions and impaired fetal development, with many reports indicating tobacco-associated morbidity and perinatal mortality. In our study, an experimental rat model of diabetes and cigarette smoke exposure in pregnant rats was used to determine the impact of the combination of diabetes and exposure to cigarette smoke during pregnancy on maternal oxidative stress biomarkers and placental and fetal development. Diabetes was induced by streptozotocin, and dams were exposed to cigarette smoke by mainstream smoke generated by a mechanical smoking device and delivered into a chamber. Four groups of dams were studied: nondiabetic (C, control) and diabetic (D) exposed to filtered air and nondiabetic (CS) and diabetic (DS) exposed to cigarette smoke prior to and during pregnancy. Maternal oxidative stress biomarkers, placental morphology, and fetal growth were determined close to term. The combination of diabetes and cigarette smoke resulted in elevated maternal blood glucose levels and increased number of small fetuses. Placentas from the DS group showed increased junctional zone and decreased labyrinthine area. The morphological alterations were characterized by extensive vascular congestion, thickness, and hyalinization of the vascular walls, numerous decidual cells with abundant glycogen, and macrophages with cytoplasmic inclusions of hemosiderin. Additionally, they showed increased glycogen accumulation and junctional zone structural derangement with ectopic giant cells. No alterations were observed in maternal oxidative stress status. Thus, our result suggests that diabetes makes pregnant rats more susceptible to the adverse effects of exposure to cigarette smoke on placental morphometry and fetal growth.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Herrera E. Implications of dietary fatty acids during pregnancy on placental, fetal and postnatal development—a review. Placenta. 2002;23(suppl A):S9–S19.

    Article  PubMed  Google Scholar 

  2. Illsley NP. Glucose transporters in the human placenta. Placenta. 2000;21(1):14–22.

    Article  CAS  PubMed  Google Scholar 

  3. Gauster M, Desoye G, Tötsch M, Hiden U. The placenta and gestational diabetes mellitus. Curr Diab Rep. 2012;12(1):16–23.

    Article  CAS  PubMed  Google Scholar 

  4. Huynh J, Yamada J, Beauharnais C, et al. Type 1, type 2 and gestational diabetes mellitus differentially impact placental pathologic characteristics of uteroplacental malperfusion. Placenta. 2015;36(10):1161–1166.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Akison LK, Nitert MD, Clifton VL, Moritz KM, Simmons DG. Review: alterations in placental glycogen deposition in complicated pregnancies: current preclinical and clinical evidence. Placenta. 2017;54:52–58. doi:https://doi.org/10.1016/j.placenta.2017.01.114

    Article  CAS  PubMed  Google Scholar 

  6. National Center for Chronic Disease Prevention and Health Promotion (US) Office on Smoking and Health. The health consequences of smoking—50 years of progress: a report of the surgeon general. Atlanta, GA: Centers for Disease Control and Prevention (US); 2014; 9, Reproductive Outcomes.

  7. Florek E, Marszalek A. An experimental study of the influences of tobacco smoke on fertility and reproduction. Hum Exp Toxicol. 1999;18(4):272–278.

    Article  CAS  PubMed  Google Scholar 

  8. van Oppenraaij RHF, Koning AHJ, van den Hoff MJB, van der Spek PJ, Steegers EAP, Exalto N. The effect of smoking on early chorionic villous vascularization. Placenta. 2012;33(88):645–651.

    Article  PubMed  Google Scholar 

  9. Czekaj P, Palasz A, Lebda-Wyborny T, et al. Morphological changes in lungs, placenta, liver, and kidneys of pregnant rats exposed to cigarette smoke. Int Arch Occup Environ Health. 2002;75(suppl):S27–S35.

    CAS  PubMed  Google Scholar 

  10. Haire-Joshu D, Glasgow RE, Tibbs TL. Smoking and diabetes. Diabetes Care. 1999;22(11):1887–1898.

    Article  CAS  PubMed  Google Scholar 

  11. Damasceno DC, Volpato GT, Sinzato YK, et al. Genotoxicity and fetal abnormality in streptozotocin-induced diabetic rats exposed to cigarette smoke prior to and during pregnancy. Exp Clin Endocrinol Diabetes. 2011;119(9):549–553.

    Article  CAS  PubMed  Google Scholar 

  12. Damasceno DC, Sinzato YK, Lima PH, et al. Effects of exposure to cigarette smoke prior to pregnancy in diabetic rats. Diabetol Metab Syndr. 2011;3(1):20. doi:https://doi.org/10.1186/1758-5996-3-20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Afiune LAF, Leal-Silva T, Sinzato YK, et al. Beneficial effects of Hibiscus rosa-sinensis L. flower aqueous extract in pregnant rats with diabetes. PLoS One. 2017;12(6):e0179785.

    Article  PubMed  PubMed Central  Google Scholar 

  14. de Souza Mda S, Sinzato YK, Lima PH, Calderon IM, Rudge MV, Damasceno DC. Oxidative stress status and lipid profiles of diabetic pregnant rats exposed to cigarette smoke. Reprod Biomed Online. 2010;20(4):547–552.

    Article  PubMed  Google Scholar 

  15. Mori M, Bogdan A, Balassa T, Csabai T, Szekeres-Bartho J. The decidua—the maternal bed embracing the embryo—maintains the pregnancy. Semin Immunopathol. 2016;38(6):635–649.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Deanesly R. Termination of early pregnancy in rats after ovariectomy is due to immediate collapse of the progesterone-dependent decidua. J Reprod Fertil. 1973;35(1):183–186.

    Article  CAS  PubMed  Google Scholar 

  17. Brosens JJ, Gellersen B. Death or survival—progesterone-dependent cell fate decisions in the human endometrial stroma. J Mol Endocrinol. 2006;36(3):389–398.

    Article  CAS  PubMed  Google Scholar 

  18. Lee KY, DeMayo FJ. Animal models of implantation. Reproduction. 2004;128(6):679–695.

    Article  CAS  PubMed  Google Scholar 

  19. Garris DR. Effects of diabetes on uterine condition, decidualization, vascularization, and corpus luteum function in the pseudopregnant rat. Endocrinol. 1988;122(2):665–672.

    Article  CAS  Google Scholar 

  20. Cuckle HS, Wald NJ, Densem JW, et al. The effect of smoking in pregnancy on maternal serum alpha-fetoprotein, unconjugated oestriol, human chorionic gonadotrophin, progesterone and dehydroepiandrosterone sulphate levels. Br J Obstet Gynaecol. 1990;97(3):272–276.

    Article  CAS  PubMed  Google Scholar 

  21. Jollie WP. Fine structural changes in placental labyrinth of the rat with increasing gestational age. J Ultrastruct Res. 1964;10:27–47. PMID: 14124029.

    Article  CAS  PubMed  Google Scholar 

  22. Sherman M. Endocrinology of rodent trophoblast cells. In: Loke Y, Whyte A, eds. Biology of Trophoblast. Amsterdam, the Netherlands: Elsevier; 1983:401–467.

    Google Scholar 

  23. Salafia C, Shiverick K. Cigarette smoking and pregnancy II: vascular effects. Placenta. 1999;20(4):273–279.

    Article  CAS  PubMed  Google Scholar 

  24. Zdravkovic T, Genbacev O, McMaster MT, Fisher SJ. The adverse effects of maternal smoking on the human placenta: a review. Placenta. 2005;26(suppl A):S81–S86.

    Article  PubMed  Google Scholar 

  25. Wu Y, Chen X, Zhou Q, et al. ITE and TCDD differentially regulate the vascular remodeling of rat placenta via the activation of AhR. PLoS One. 2014;9(1):e86549.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Soares MJ, Chakraborty D, Karim Rumi MA, Konno T, Renaud SJ. Rat placentation: an experimental model for investigating the hemochorial maternal-fetal interface. Placenta. 2012;33(4):233–243.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Soares MJ, Faria TN, Roby KF, Deb S. Pregnancy and the prolactin family of hormones: coordination of anterior pituitary, uterine, and placental expression. Endocr Rev. 1991;12(4):402–423.

    Article  CAS  PubMed  Google Scholar 

  28. Soares MJ. The prolactin and growth hormone families: pregnancy-specific hormones/cytokines at the maternal-fetal interface. Reprod Biol Endocrinol. 2004;2(1):51. doi:https://doi.org/10.1186/1477-7827-2-51

    Article  PubMed  PubMed Central  Google Scholar 

  29. Spellacy WN, Buhi WC, Birk SA. The effect of smoking on serum human placental lactogen levels. Am J Obstet Gynecol. 1977;127(3):232–234.

    Article  CAS  PubMed  Google Scholar 

  30. Campbell WJ, Deb S, Kwok SC, Joslin JA, Soares MJ. Differential expression of placental lactogen-II and prolactin-like protein-A in the rat chorioallantoic placenta. Endocrinol. 1989;125(3):1565–1574.

    Article  CAS  Google Scholar 

  31. Clapp C, Martial JA, Guzman RC, Rentier-Delure F, Weiner RI. The 16-kilodalton N-terminal fragment of human prolactin is a potent inhibitor of angiogenesis. Endocrinol. 1993;133(3):1292–1299.

    Article  CAS  Google Scholar 

  32. Jackson D, Volpert OV, Bouck N, Linzer DIH. Stimulation and inhibition of angiogenesis by placental proliferin and proliferin-related protein. Science. 1994;266(5190):1581–1584.

    Article  CAS  PubMed  Google Scholar 

  33. Michaud S, Ménard C, Guy L, Gennaro G, Rivard A. Inhibition of hypoxia-induced angiogenesis by cigarette smoke exposure: impairment of the HIF-1α/VEGF pathway. FASEB J. 2003;17(9):1150–1152.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Experimental Research on Gynecology and Obstetrics, Botucatu Medical School, Sao Paulo State University (UNESP), Botucatu, São Paulo, Brazil

    Yuri K. Sinzato PhD, Gustavo T. Volpato PhD, Marilza V. C. Rudge PhD & Débora Cristina Damasceno PhD

  2. Department of Cell and Developmental Biology, Institute of Biomedical Sciences, University of São Paulo (USP), São Paulo, Brazil

    Estela M. Bevilacqua PhD

  3. Laboratory of System Physiology and Reproductive Toxicology, Institute of Biological and Health Sciences, Federal University of Mato Grosso (UFMT), Mato Grosso, Brazil

    Gustavo T. Volpato PhD

  4. Experimental Pathology Section, Department of Pathology, National Institute of Medical Sciences and Nutrition, Mexico city, Mexico

    Rogelio E. Hernandez-Pando PhD

Authors
  1. Yuri K. Sinzato PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Estela M. Bevilacqua PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gustavo T. Volpato PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rogelio E. Hernandez-Pando PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marilza V. C. Rudge PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Débora Cristina Damasceno PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Débora Cristina Damasceno PhD.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sinzato, Y.K., Bevilacqua, E.M., Volpato, G.T. et al. Maternal Oxidative Stress, Placental Morphometry, and Fetal Growth in Diabetic Rats Exposed to Cigarette Smoke. Reprod. Sci. 26, 1287–1293 (2019). https://doi.org/10.1177/1933719118815589

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1177/1933719118815589

Keywords

Search

Navigation