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Article

Prenatal nicotine exposure induces gender-associated left ventricular-arterial uncoupling in adult offspring

  • Authors:
    • Zhenhua Wang
    • Qiufang Ouyang
    • Ziyang Huang
    • Ling Lin
    • Er'mei Yu
    • Markus W. Ferrari
  • View Affiliations / Copyright

    Affiliations: Cardiovascular Department, Second Affiliated Hospital and Second Clinical Medical College, Fujian Medical University, Quanzhou, Fujian 362000, P.R. China, Rheumatism Department, Second Affiliated Hospital and Second Clinical Medical College, Fujian Medical University, Quanzhou, Fujian 362000, P.R. China, Clinic of Internal Medicine 1, HSK, Clinic of the City of Wiesbaden and the HELIOS Group, Wiesbaden D‑65199, Germany
  • Pages: 410-418
    |
    Published online on: February 17, 2015
       https://doi.org/10.3892/mmr.2015.3364
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Abstract

Alterations in vascular or myocardial structure and function have been demonstrated in offspring subjected to prenatal nicotine exposure (PNE), however, limited data are available on how these changes interact. The present study assessed the hypothesis that prenatal nicotine exposure induced gender‑specific alterations of left ventricular‑arterial coupling indices in adult offspring. Female Sprague‑Dawley rats were exposed to either nicotine (8 mg/kg/day) or saline via subcutaneous osmotic mini‑pumps throughout gestation. Male and female offspring, aged 12 months, underwent non‑invasive echocardiography and invasive left ventricular cannulation. Left ventricular‑arterial coupling was analysed as the ratio of effective arterial elastance (Ea) to ventricular end‑systolic elastance (Ees). The left ventricular myocardium and aorta were stained with hematoxylin and eosin and the myocardial cell cross‑sectional area was calculated. Simultaneously, the ratio of medium thickness to internal diameter in the aorta and mesenteric artery was determined. The fibrosis component of left ventricle myocardium was analyzed by Sirius‑red staining and further confirmed by hydroxyproline determination. The elastic properties of the aortic wall were analyzed by van Gieson staining. PNE caused significant increases in pulse pressure (56.36±7.41 vs. 50.16±4.94 mmHg; P<0.05) and left ventricular meridional wall stress (78.25±9.12 vs. 69.64±7.58 kdyne/cm2; P<0.05) in male offspring compared with the control. Conversely, no similar effect was observed in female offspring. An elevated augmentation index was noted in male and female pups. Additionally, Ea/Ees was reduced in PNE males compared with control males, due to a disproportionate increase in Ees vs. Ea whereas in females, Ea/Ees did not differ significantly due to tandem increase in Ea and Ees. In addition, collagen cross‑linking was markedly higher in male offspring, whereas it was unaltered in females compared with their respective controls. Fragmentation of the elastic network in the aorta and the increased ratio of medial thickness to internal diameter in the mesenteric artery were more evident in male offspring when compared with female offspring. PNE caused combined ventricular‑arterial stiffening in male and female offspring, with lower Ea/Ees in males, while Ea/Ees was preserved in females. Enhanced collagen cross‑linking in the myocardium, underdeveloped elastic fibers in the aorta and remodeled resistance vessels were associated with pathological ventricular arterial mismatching. The results of the present study indicated that male offspring were more susceptible to the development of ventricular and arterial dysfunction in response to PNE compared with female offspring.
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1 

Hanna ST: Nicotine effect on cardiovascular system and ion channels. J Cardiovasc Pharmacol. 47:348–358. 2006.PubMed/NCBI

2 

Benowitz NL and Gourlay SG: Cardiovascular toxicity of nicotine: implications for nicotine replacement therapy. J Am Coll Cardiol. 29:1422–1431. 1997. View Article : Google Scholar : PubMed/NCBI

3 

Wang Z, Huang Z, Lu G, et al: Hypoxia during pregnancy in rats leads to early morphological changes of atherosclerosis in adult offspring. Am J Physiol Heart Circ Physiol. 296:H1321–H1328. 2009. View Article : Google Scholar : PubMed/NCBI

4 

Gao YJ, Holloway AC, Zeng ZH, et al: Prenatal exposure to nicotine causes postnatal obesity and altered perivascular adipose tissue function. Obes Res. 13:687–692. 2005. View Article : Google Scholar : PubMed/NCBI

5 

Rueda-Clausen CF, Morton JS and Davidge ST: Effects of hypoxia-induced intrauterine growth restriction on cardiopulmonary structure and function during adulthood. Cardiovasc Res. 81:713–722. 2009. View Article : Google Scholar

6 

Lawrence J, Xiao D, Xue Q, et al: Prenatal nicotine exposure increases heart susceptibility to ischemia/reperfusion injury in adult offspring. J Pharmacol Exp Ther. 324:331–341. 2008. View Article : Google Scholar

7 

Gao YJ, Holloway AC, Su LY, et al: Effects of fetal and neonatal exposure to nicotine on blood pressure and perivascular adipose tissue function in adult life. Eur J Pharmacol. 590:264–268. 2008. View Article : Google Scholar : PubMed/NCBI

8 

Xiao D, Huang X, Lawrence J, et al: Fetal and neonatal nicotine exposure differentially regulates vascular contractility in adult male and female offspring. J Pharmacol Exp Ther. 320:654–661. 2007. View Article : Google Scholar

9 

Kim JW, Park CG, Hong SJ, et al: Acute and chronic effects of cigarette smoking on arterial stiffness. Blood Press. 14:80–85. 2005. View Article : Google Scholar : PubMed/NCBI

10 

Goette A, Lendeckel U, Kuchenbecker A, et al: Cigarette smoking induces atrial fibrosis in humans via nicotine. Heart. 3:1056–1063. 2007. View Article : Google Scholar

11 

Rajiyah G, Agarwal R, Avendano G, et al: Influence of nicotine on myocardial stiffness and fibrosis during chronic ethanol use. Alcohol Clin Exp Res. 20:985–989. 1996. View Article : Google Scholar : PubMed/NCBI

12 

Fourie PR, Coetzee AR and Bolliger CT: Pulmonary artery compliance: its role in right ventricular-arterial coupling. Cardiovasc Res. 26:839–844. 1992. View Article : Google Scholar : PubMed/NCBI

13 

Boychuk CR and Hayward LF: Prenatal nicotine exposure alters postnatal cardiorespiratory integration in young male but not female rats. Exp Neurol. 232:212–221. 2011. View Article : Google Scholar : PubMed/NCBI

14 

Fennessy F, Casey RG and Bouchier-Hayes D: Peripheral and central arterial haemodynamic interactions are early abnormalities in young male cigarette smokers. Eur J Vasc Endovasc Surg. 25:152–158. 2003. View Article : Google Scholar : PubMed/NCBI

15 

Xiao D, Xu Z, Huang X, et al: Prenatal gender-related nicotine exposure increases blood pressure response to angiotensin II in adult offspring. Hypertension. 51:1239–1247. 2008. View Article : Google Scholar : PubMed/NCBI

16 

Sumitra M, Manikandan P, Rao KV, et al: Cardiorespiratory effects of diazepam-ketamine, xylazine-ketamine and thiopentone anesthesia in male Wistar rats - a comparative analysis. Life Sci. 75:1887–1896. 2004. View Article : Google Scholar : PubMed/NCBI

17 

Jegger D, da Silva R, Jeanrenaud X, et al: Ventricular-arterial coupling in a rat model of reduced arterial compliance provoked by hypervitaminosis D and nicotine. Am J Physiol Heart Circ Physiol. 291:H1942–H1951. 2006. View Article : Google Scholar : PubMed/NCBI

18 

Weinberg EO, Thienelt CD, Katz SE, et al: Gender differences in molecular remodeling in pressure overload hypertrophy. J Am Coll Cardiol. 34:264–273. 1999. View Article : Google Scholar : PubMed/NCBI

19 

Sahlén A, Shahgaldi K, Aagaard P, et al: Altered ventriculo-arterial coupling during exercise in athletes releasing biomarkers after endurance running. Eur J Appl Physiol. 112:4069–4079. 2012. View Article : Google Scholar : PubMed/NCBI

20 

Blaudszun G and Morel DR: Relevance of the volume-axis intercept, V0, compared with the slope of end-systolic pressure-volume relationship in response to large variations in inotropy and afterload in rats. Exp Physiol. 96:1179–1195. 2011. View Article : Google Scholar : PubMed/NCBI

21 

London GM, Blacher J, Pannier B, et al: Arterial wave reflections and survival in end-stage renal failure. Hypertension. 38:434–438. 2001. View Article : Google Scholar : PubMed/NCBI

22 

Lartaud I, Gaillard V, Dauca M, et al: Pioglitazone protects against elastocalcinosis and improves aortic wall elasticity. Ann Pharm Fr. 65:189–194. 2007.In French. View Article : Google Scholar : PubMed/NCBI

23 

Leipner C, Grün K, Müller A, et al: Imatinib mesylate attenuates fibrosis in coxsackievirus b3-induced chronic myocarditis. Cardiovasc Res. 79:118–126. 2008. View Article : Google Scholar : PubMed/NCBI

24 

Marque V, Kieffer P, Gayraud B, et al: Aortic wall mechanics and composition in a transgenic mouse model of Marfan syndrome. Arterioscler Thromb Vasc Biol. 21:1184–1189. 2001. View Article : Google Scholar : PubMed/NCBI

25 

Yamamoto K, Masuyama T, Sakata Y, et al: Myocardial stiffness is determined by ventricular fibrosis, but not by compensatory or excessive hypertrophy in hypertensive heart. Cardiovasc Res. 55:76–82. 2002. View Article : Google Scholar : PubMed/NCBI

26 

do Carmo Pinho Franco M, Nigro D, Fortes ZB, et al: Intrauterine undernutrition - renal and vascular origin of hypertension. Cardiovasc Res. 60:228–234. 2003. View Article : Google Scholar : PubMed/NCBI

27 

Xiao D, Huang X, Yang S and Zhang L: Estrogen normalizes perinatal nicotine-induced hypertensive responses in adult female rat offspring. Hypertension. 61:1246–1254. 2013. View Article : Google Scholar : PubMed/NCBI

28 

Heffernan KS, Patvardhan EA, Hession M, et al: Elevated augmentation index derived from peripheral arterial tonometry is associated with abnormal ventricular-vascular coupling. Clin Physiol Funct Imaging. 30:313–317. 2010.PubMed/NCBI

29 

Sassalos K, Vlachopoulos C, Alexopoulos N, et al: The acute and chronic effect of cigarette smoking on the elastic properties of the ascending aorta in healthy male subjects. Hellenic J Cardiol. 47:263–268. 2006.PubMed/NCBI

30 

Norton GR, Tsotetsi J, Trifunovic B, et al: Myocardial stiffness is attributed to alterations in cross-linked collagen rather than total collagen or phenotypes in spontaneously hypertensive rats. Circulation. 96:1991–1998. 1997. View Article : Google Scholar : PubMed/NCBI

31 

Antonini-Canterin F, Carerj S, Di Bello V, et al: Arterial stiffness and ventricular stiffness: a couple of diseases or a coupling disease? A review from the cardiologist’s point of view. Eur J Echocardiogr. 10:36–43. 2009. View Article : Google Scholar

32 

Frenneaux M and Williams L: Ventricular-arterial and ventricular-ventricular interactions and their relevance to diastolic filling. Prog Cardiovasc Dis. 49:252–262. 2007. View Article : Google Scholar

33 

Xue Q and Zhang L: Prenatal hypoxia causes a sex-dependent increase in heart susceptibility to ischemia and reperfusion injury in adult male offspring: role of protein kinase C epsilon. J Pharmacol Exp Ther. 330:624–632. 2009. View Article : Google Scholar : PubMed/NCBI

34 

Goette A: Nicotine, atrial fibrosis and atrial fibrillation: do microRNAs help to clear the smoke? Cardiovasc Res. 83:421–422. 2009. View Article : Google Scholar : PubMed/NCBI

35 

Lawrence J, Chen M, Xiong F, et al: Foetal nicotine exposure causes PKCε gene repression by promoter methylation in rat hearts. Cardiovasc Res. 89:89–97. 2011. View Article : Google Scholar

36 

Chen CH, Fetics B, Nevo E, et al: Noninvasive single-beat determination of left ventricular end-systolic elastance in humans. J Am Coll Cardiol. 38:2028–2034. 2001. View Article : Google Scholar : PubMed/NCBI

37 

Kato S, Spinale FG, Tanaka R, et al: Inhibition of collagen cross-linking: effects on fibrillar collagen and ventricular diastolic function. Am J Physiol. 269(3 Pt 2): H863–H868. 1995.PubMed/NCBI

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Copy and paste a formatted citation
Spandidos Publications style
Wang Z, Ouyang Q, Huang Z, Lin L, Yu E and Ferrari MW: Prenatal nicotine exposure induces gender-associated left ventricular-arterial uncoupling in adult offspring. Mol Med Rep 12: 410-418, 2015.
APA
Wang, Z., Ouyang, Q., Huang, Z., Lin, L., Yu, E., & Ferrari, M.W. (2015). Prenatal nicotine exposure induces gender-associated left ventricular-arterial uncoupling in adult offspring. Molecular Medicine Reports, 12, 410-418. https://doi.org/10.3892/mmr.2015.3364
MLA
Wang, Z., Ouyang, Q., Huang, Z., Lin, L., Yu, E., Ferrari, M. W."Prenatal nicotine exposure induces gender-associated left ventricular-arterial uncoupling in adult offspring". Molecular Medicine Reports 12.1 (2015): 410-418.
Chicago
Wang, Z., Ouyang, Q., Huang, Z., Lin, L., Yu, E., Ferrari, M. W."Prenatal nicotine exposure induces gender-associated left ventricular-arterial uncoupling in adult offspring". Molecular Medicine Reports 12, no. 1 (2015): 410-418. https://doi.org/10.3892/mmr.2015.3364
Copy and paste a formatted citation
x
Spandidos Publications style
Wang Z, Ouyang Q, Huang Z, Lin L, Yu E and Ferrari MW: Prenatal nicotine exposure induces gender-associated left ventricular-arterial uncoupling in adult offspring. Mol Med Rep 12: 410-418, 2015.
APA
Wang, Z., Ouyang, Q., Huang, Z., Lin, L., Yu, E., & Ferrari, M.W. (2015). Prenatal nicotine exposure induces gender-associated left ventricular-arterial uncoupling in adult offspring. Molecular Medicine Reports, 12, 410-418. https://doi.org/10.3892/mmr.2015.3364
MLA
Wang, Z., Ouyang, Q., Huang, Z., Lin, L., Yu, E., Ferrari, M. W."Prenatal nicotine exposure induces gender-associated left ventricular-arterial uncoupling in adult offspring". Molecular Medicine Reports 12.1 (2015): 410-418.
Chicago
Wang, Z., Ouyang, Q., Huang, Z., Lin, L., Yu, E., Ferrari, M. W."Prenatal nicotine exposure induces gender-associated left ventricular-arterial uncoupling in adult offspring". Molecular Medicine Reports 12, no. 1 (2015): 410-418. https://doi.org/10.3892/mmr.2015.3364
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